[Federal Register Volume 78, Number 189 (Monday, September 30, 2013)]
[Proposed Rules]
[Pages 60023-60098]
From the Federal Register Online via the Government Printing Office [www.gpo.gov]
[FR Doc No: 2013-22700]

[[Page 60023]]

Vol. 78


No. 189

September 30, 2013

Part II

Department of the Interior


Fish & Wildlife Service


50 CFR Part 17

Endangered and Threatened Wildlife and Plants; Proposed Threatened 
Status for the Rufa Red Knot (Calidris canutus rufa); Proposed Rule

Federal Register / Vol. 78, No. 189 / Monday, September 30, 2013 / 
Proposed Rules

[[Page 60024]]



Fish and Wildlife Service

50 CFR Part 17

[Docket No. FWS-R5-ES-2013-0097; 4500030113]
RIN 1018-AY17

Endangered and Threatened Wildlife and Plants; Proposed 
Threatened Status for the Rufa Red Knot (Calidris canutus rufa)

AGENCY: Fish and Wildlife Service, Interior.

ACTION: Proposed rule.


SUMMARY: We, the U.S. Fish and Wildlife Service, propose to list the 
rufa red knot (Calidris canutus rufa) as a threatened species under the 
Endangered Species Act of 1973, as amended (Act). If we finalize this 
rule as proposed, it would extend the Act's protections to this 
species. The effect of this regulation will be to add this species to 
the List of Endangered and Threatened Wildlife.

DATES: We will accept all comments received or postmarked on or before 
November 29, 2013. Comments submitted electronically using the Federal 
eRulemaking Portal (see ADDRESSES section, below) must be received by 
11:59 p.m. Eastern Time on the closing date. We must receive requests 
for public hearings, in writing, at the address shown in the FOR 
FURTHER INFORMATION CONTACT section by November 14, 2013.

ADDRESSES: Document availability: You may obtain copies of the proposed 
rule and its four supplemental documents on the Internet at http://www.regulations.gov at Docket Number FWS-R5-ES-2013-0097, or by mail 
from the New Jersey Field Office (see FOR FURTHER INFORMATION CONTACT).
    Comment submission: You may submit written comments by one of the 
following methods:
    (1) Electronically: Go to the Federal eRulemaking Portal: http://www.regulations.gov. In the Search box, enter FWS-R5-ES-2013-0097, 
which is the docket number for this rulemaking. You may submit a 
comment by clicking on ``Comment Now!''
    (2) By hard copy: Submit by U.S. mail or hand-delivery to: Public 
Comments Processing, Attn: FWS-R5-ES-2013-0097; Division of Policy and 
Directives Management; U.S. Fish and Wildlife Service; 4401 N. Fairfax 
Drive, MS 2042-PDM; Arlington, Virginia 22203.
    We request that you send comments only by the methods described 
above. We will post all information received on http://www.regulations.gov. This generally means that we will post any 
personal information you provide us (see the Public Comments section 
below for more details).

Supervisor, U.S. Fish and Wildlife Service, New Jersey Field Office, 
927 North Main Street, Building D, Pleasantville, New Jersey 08232, by 
telephone 609-383-3938 or by facsimile 609-646-0352. Persons who use a 
telecommunications device for the deaf (TDD) may call the Federal 
Information Relay Service (FIRS) at 800-877-8339.


Executive Summary

    Why we need to publish a rule. Under the Act, if a species is 
determined to be endangered or threatened throughout all or a 
significant portion of its range, we are required to promptly publish a 
proposal in the Federal Register and make a determination on our 
proposal within 1 year. Critical habitat shall be designated, to the 
maximum extent prudent and determinable, for any species determined to 
be an endangered or threatened species under the Act. Listing a species 
as an endangered or threatened species and designations and revisions 
of critical habitat can be completed only by issuing a rule.
    This rule proposes listing the rufa red knot (Calidris canutus 
rufa) as a threatened species. The rufa red knot is a candidate species 
for which we have on file sufficient information on biological 
vulnerability and threats to support preparation of a listing proposal, 
but for which development of a listing regulation has been precluded by 
other higher priority listing activities. This rule reassesses all 
available information regarding status of and threats to the rufa red 
knot. We will also publish a proposal to designate critical habitat for 
the rufa red knot under the Act in the near future.
    The basis for our action. Under the Act, we may determine that a 
species is an endangered or threatened species based on any of five 
factors: (A) The present or threatened destruction, modification, or 
curtailment of its habitat or range; (B) Overutilization for 
commercial, recreational, scientific, or educational purposes; (C) 
Disease or predation; (D) The inadequacy of existing regulatory 
mechanisms; or (E) Other natural or manmade factors affecting its 
continued existence.
    We have determined that the rufa red knot is threatened due to loss 
of both breeding and nonbreeding habitat; potential for disruption of 
natural predator cycles on the breeding grounds; reduced prey 
availability throughout the nonbreeding range; and increasing frequency 
and severity of asynchronies (``mismatches'') in the timing of the 
birds' annual migratory cycle relative to favorable food and weather 
    We will seek peer review. We will seek comments from independent 
specialists to ensure that our designation is based on scientifically 
sound data, assumptions, and analyses. We will invite these peer 
reviewers to comment on our listing proposal. Because we will consider 
all comments and information received during the comment period, our 
final determinations may differ from this proposal.

Information Requested

Public Comments

    We intend that any final action resulting from this proposed rule 
will be based on the best scientific and commercial data available and 
be as accurate and as effective as possible. Therefore, we request 
comments or information from the public, other concerned governmental 
agencies, Native American tribes, the scientific community, industry, 
or any other interested parties concerning this proposed rule. We 
particularly seek comments concerning:
    (1) The rufa red knot's biology, range, and population trends, 
    (a) Biological or ecological requirements of the species, including 
habitat requirements for feeding, breeding, and sheltering;
    (b) Genetics and taxonomy;
    (c) Historical and current range including distribution patterns;
    (d) Historical and current population levels and current and 
projected trends; and
    (e) Past and ongoing conservation measures for the species, its 
habitat, or both.
    (2) Factors that that may affect the continued existence of the 
species, which may include habitat modification or destruction, 
overutilization, disease, predation, the inadequacy of existing 
regulatory mechanisms, or other natural or manmade factors.
    (3) Biological, commercial trade, or other relevant data concerning 
any threats (or lack thereof) to this species and regulations that may 
be addressing those threats.
    (4) Additional information concerning the historical and current 
status, range, distribution, and population size of this species, 
including the locations of any additional populations of this species.

[[Page 60025]]

    (5) Genetic, morphological, chemical, geolocator, telemetry, survey 
(e.g., resightings of marked birds), or other data that clarify the 
distribution of Calidris canutus rufa versus C.c. roselaari wintering 
and migration areas, including the subspecies compositions of those C. 
canutus that occur from southern Mexico to the Caribbean and Pacific 
coasts of South America.
    (6) Information regarding intra- and inter-annual red knot 
movements within and between the Southeast United States-Caribbean and 
the Northwest Gulf of Mexico wintering regions, or other information 
that helps to clarify their geographic limits and degree of 
    (7) Information that helps clarify the geographic extent of the 
rufa red knot's breeding range, and the extent to which rufa red knots 
from different wintering areas interbreed, as well as the geographic 
extent of the Calidris canutus islandica breeding range.
    (8) Data regarding rates of rufa red knot reproductive success.
    (9) Information regarding habitat loss or predation in rufa red 
knot breeding areas.
    (10) Information regarding important rufa red knot stopover areas, 
including inland areas (such as the Mississippi Valley, Great Lakes, 
and Great Plains). We particularly seek information on the frequency, 
timing, and duration of use; numbers of birds; habitat and prey 
characteristics; foraging and roosting habits; and any threats 
associated with such areas.
    (11) Data that support or refute the concept that juvenile rufa red 
knots at least partially segregate from adults during the nonbreeding 
seasons. We particularly seek information on juvenile wintering and 
migration locations; frequency, timing, and duration of juvenile use; 
numbers of juveniles and adults in these areas; juvenile habitat and 
prey characteristics; juvenile foraging and roosting habits; juvenile 
survival rates; and any threats associated with these areas.
    (12) Data that clarify the degree of rufa red knot site fidelity to 
breeding locations, wintering regions, or migration stopover sites.
    (13) Data regarding the percentage of rufa red knots that do not 
use Delaware Bay as a spring stopover site.
    (14) Data regarding rufa red knot use of the Caribbean. We 
particularly seek information on the frequency, timing, and duration of 
use; numbers of birds; habitat and prey characteristics; foraging and 
roosting habits; and any threats associated with areas of red knot use 
in the Caribbean.
    (15) Data regarding red knot use of wrack material as a 
microhabitat for foraging or roosting.
    (16) Information regarding the frequency and severity of the 
threats to red knots (e.g., documented mortality levels from disease, 
harmful algal blooms, contaminants, oil spills, wind turbines), their 
habitats (e.g., effects of sea level rise, development, aquaculture), 
or their food resources (e.g., harvest of marine resources, climate 
change) outside the United States.
    (17) Information regarding legal and illegal harvest (i.e., hunting 
or poaching) rates and trends in nonbreeding areas and the effects of 
harvest on the red knot.
    (18) Information regarding non-U.S. laws, regulations, or policies 
relevant to the regulation of red knot hunting; classification of the 
red knot as a protected species; protection of red knot habitats; or 
threats to the red knot (e.g., to address the data gaps identified 
under Summary of Factors Affecting the Species).
    Please include sufficient information with your submission (such as 
scientific journal articles or other publications) to allow us to 
verify any scientific or commercial information you include.
    Please note that submissions merely stating support for or 
opposition to the action under consideration without providing 
supporting information, although noted, will not be considered in 
making a determination, as section 4(b)(1)(A) of the Act directs that 
determinations as to whether any species is an endangered or threatened 
species must be made ``solely on the basis of the best scientific and 
commercial data available.''
    You may submit your comments and materials concerning this proposed 
rule by one of the methods listed in the ADDRESSES section. We request 
that you send comments only by the methods described in the ADDRESSES 
    If you submit information via http://www.regulations.gov, your 
entire submission--including any personal identifying information--will 
be posted on the Web site. If your submission is made via a hardcopy 
that includes personal identifying information, you may request at the 
top of your document that we withhold this information from public 
review. However, we cannot guarantee that we will be able to do so. We 
will post all hardcopy submissions on http://www.regulations.gov. 
Please include sufficient information with your comments to allow us to 
verify any scientific or commercial information you include.
    Comments and materials we receive, as well as supporting 
documentation we used in preparing this proposed rule, will be 
available for public inspection on http://www.regulations.gov, or by 
appointment, during normal business hours, at the U.S. Fish and 
Wildlife Service, New Jersey Field Office (http://www.fws.gov/northeast/njfieldoffice/) (see FOR FURTHER INFORMATION CONTACT).

Public Hearings

    Section 4(b)(5) of the Act provides for one or more public hearings 
on this proposal, if requested. Requests must be received within 45 
days after the date of publication of this proposed rule in the Federal 
Register. Such requests must be sent to the address shown in the FOR 
FURTHER INFORMATION CONTACT section. We will schedule public hearings 
on this proposal, if any are requested, and announce the dates, times, 
and places of those hearings, as well as how to obtain reasonable 
accommodations, in the Federal Register and local newspapers at least 
15 days before the hearing.
    Persons needing reasonable accommodations to attend and participate 
in a public hearing should contact the New Jersey Field Office at 609-
383-3938, as soon as possible. To allow sufficient time to process 
requests, please call no later than 1 week before any scheduled hearing 
date. Information regarding this proposed rule is available in 
alternative formats upon request.

Peer Review

    In accordance with our joint policy on peer review published in the 
Federal Register on July 1, 1994 (59 FR 34270), we have sought the 
expert opinions of three appropriate and independent specialists 
regarding this proposed rule. The purpose of peer review is to ensure 
that our listing determination and critical habitat designation are 
based on scientifically sound data, assumptions, and analyses. The peer 
reviewers have expertise in the red knot's biology, habitat, or 
threats, which will inform our determination. We invite comment from 
the peer reviewers during this public comment period.

Previous Federal Action

    Comprehensive information regarding previous federal actions 
relevant to the proposed listing of the rufa red knot is available as a 
supplemental document (``Previous Federal Actions'') on the Internet at 
http://www.regulations.gov (Docket No. FWS-R5-ES-2013-0097; see 
ADDRESSES section for further access instructions).

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Species Information

    Comprehensive information regarding the rufa red knot's taxonomy, 
distribution, life history, habitat, and diet, as well as its 
historical and current abundance, is available as a supplemental 
document (``Rufa Red Knot Ecology and Abundance'') on the Internet at 
http://www.regulations.gov (Docket No. FWS-R5-ES-2013-0097; see 
ADDRESSES section for further access instructions). A brief summary is 
provided here.
    The rufa red knot (Calidris canutus rufa) is a medium-sized 
shorebird about 9 to 11 inches (in) (23 to 28 centimeters (cm)) in 
length. (Throughout this document, ``rufa red knot,'' ``red knot,'' and 
``knot'' are used interchangeably to refer to the rufa subspecies. 
``Calidris canutus'' and ``C. canutus'' are used to refer to the 
species as a whole or to birds of unknown subspecies. References to 
other particular subspecies are so indicated.) The red knot migrates 
annually between its breeding grounds in the Canadian Arctic and 
several wintering regions, including the Southeast United States 
(Southeast), the Northeast Gulf of Mexico, northern Brazil, and Tierra 
del Fuego at the southern tip of South America. During both the 
northbound (spring) and southbound (fall) migrations, red knots use key 
staging and stopover areas to rest and feed.
    Calidris canutus is classified in the Class Aves, Order 
Charadriiformes, Family Scolopacidae, Subfamily Scolopacinae (American 
Ornithologists Union (AOU) 2012a). Six subspecies are recognized, each 
with distinctive morphological traits (i.e., body size and plumage 
characteristics), migration routes, and annual cycles. Each subspecies 
is believed to occupy a distinct breeding area in various parts of the 
Arctic (Buehler and Baker 2005, pp. 498-499; Tomkovich 2001, pp. 259-
262; Piersma and Baker 2000, p. 109; Piersma and Davidson 1992, p. 191; 
Tomkovich 1992, pp. 20-22), but some subspecies overlap in certain 
wintering and migration areas (Conservation of Arctic Flora and Fauna 
(CAFF) 2010, p. 33).
    Calidris canutus canutus, C.c. piersma, and C.c. rogersi do not 
occur in North America. The subspecies C.c. islandica breeds in the 
northeastern Canadian High Arctic and Greenland, migrates through 
Iceland and Norway, and winters in western Europe (Committee on the 
Status of Endangered Wildlife in Canada (COSEWIC) 2007, p. 4). Calidris 
c. rufa breeds in the central Canadian Arctic (just south of the C.c. 
islandica breeding grounds) and winters along the Atlantic coast and 
the Gulf of Mexico coast (Gulf coast) of North America, in the 
Caribbean, and along the north and southeast coasts of South America 
including the island of Tierra del Fuego at the southern tip of 
Argentina and Chile (see supplemental document--Rufa Red Knot Ecology 
and Abundance--figures 1 and 2).
    Subspecies Calidris canutus roselaari breeds in western Alaska and 
on Wrangel Island, Russia (Carmona et al. in press; Buehler and Baker 
2005, p. 498). Wintering areas for C.c. roselaari are poorly known 
(Harrington 2001, p. 5). In the past, C. canutus wintering along the 
northern coast of Brazil, the Gulf coasts of Texas and Florida, and the 
southeast Atlantic coast of the United States have sometimes been 
attributed to the roselaari subspecies. However, based on new 
morphological evidence, resightings of marked birds, and results from 
geolocators (light-sensitive tracking devices), C.c. roselaari is now 
thought to be largely or wholly confined to the Pacific coast of the 
Americas during migration and in winter (Carmona et al. in press; 
Buchanan et al. 2011, p. 97; USFWS 2011a, pp. 305-306; Buchanan et al. 
2010, p. 41; Soto-Montoya et al. 2009, p. 191; Niles et al. 2008, pp. 
131-133; Tomkovich and Dondua 2008, p. 102). Although C.c. roselaari is 
generally considered to occur on the Pacific coast, a few C. canutus 
movements have recently been documented between Texas and the Pacific 
coast during spring migration (Carmona et al. in press). Despite a 
number of population-wide morphological differences (U.S. Fish and 
Wildlife Service (USFWS) 2011a, p. 305), the rufa and roselaari 
subspecies cannot be distinguished in the field (D. Newstead pers. 
comm. September 14, 2012). The subspecies composition of Pacific-
wintering C. canutus from central Mexico to Chile is unknown.
    Pursuant to the definitions in section 3 of the Act, ``the term 
species includes any subspecies of fish or wildlife or plants, and any 
distinct population segment of any species of vertebrate fish or 
wildlife which interbreeds when mature.'' Based on the information in 
the supplemental document Rufa Red Knot Ecology and Abundance, the 
Service accepts the characterization of Calidris canutus rufa as a 
subspecies because each recognized subspecies is believed to occupy 
separate breeding areas, in addition to having morphological and 
behavioral character differences. Therefore, we find that C.c. rufa is 
a valid taxon that qualifies as a listable entity under the Act.
    Based on estimated survival rates for a stable population, few red 
knots live for more than about 7 years (Niles et al. 2008, p. 28). Age 
of first breeding is uncertain but for most birds is probably at least 
2 years (Harrington 2001, p. 21). Red knots generally nest in dry, 
slightly elevated tundra locations, often on windswept slopes with 
little vegetation. Breeding territories are located inland, but near 
arctic coasts, and foraging areas are located near nest sites in 
freshwater wetlands (Niles et al. 2008, p. 27; Harrington 2001, p. 8). 
On the breeding grounds, the red knot's diet consists mostly of 
terrestrial invertebrates such as insects (Harrington 2001, p. 11). 
Breeding occurs in June (Niles et al. 2008, pp. 25-26). Breeding 
success of High Arctic shorebirds such as Calidris canutus varies 
dramatically among years in a somewhat cyclical manner. Two main 
factors seem to be responsible for this annual variation: weather that 
affects nesting conditions and food availability (see Summary of 
Factors Affecting the Species--Factor E--Asynchronies) and the 
abundance of arctic lemmings (Dicrostonyx torquatus and Lemmus 
sibericus) that affects predation rates (see Summary of Factors 
Affecting the Species--Factor C--Predation--Breeding).
    In this document, ``winter'' is used to refer to the nonbreeding 
period of the red knot life cycle when the birds are not undertaking 
migratory movements. Red knots occupy all known wintering areas from 
December to February, but may be present in some wintering areas as 
early as September or as late as May. In the Southern Hemisphere, these 
months correspond to the austral summer (i.e., summer in the Southern 
Hemisphere), but for consistency in this document the terms ``winter'' 
and ``wintering area'' are used throughout the subspecies' range.
    Wintering areas for the red knot include the Atlantic coasts of 
Argentina and Chile (particularly the island of Tierra del Fuego that 
spans both countries), the north coast of Brazil (particularly in the 
State of Maranh[atilde]o), the Northwest Gulf of Mexico from the 
Mexican State of Tamaulipas through Texas (particularly at Laguna 
Madre) to Louisiana, and the Southeast United States from Florida 
(particularly the central Gulf coast) to North Carolina (Newstead et 
al. in press; L. Patrick pers. comm. August 31, 2012; Niles et al. 
2008, p 17) (see supplemental

[[Page 60027]]

document--Rufa Red Knot Ecology and Abundance--figure 2). Smaller 
numbers of knots winter in the Caribbean, and along the central Gulf 
coast (Alabama, Mississippi), the mid-Atlantic, and the Northeast 
United States. Calidris canutus is also known to winter in Central 
America and northwest South America, but it is not yet clear if all 
these birds are the rufa subspecies. Little information exists on where 
juvenile red knots spend the winter months (USFWS and Conserve Wildlife 
Foundation 2012, p. 1), and there may be at least partial segregation 
of juvenile and adult red knots on the wintering grounds.
    Each year red knots make one of the longest distance migrations 
known in the animal kingdom, traveling up to 19,000 miles (mi) (30,000 
kilometers (km) annually. Red knots undertake long flights that may 
span thousands of miles without stopping. As Calidris canutus prepare 
to depart on long migratory flights, they undergo several physiological 
changes. Before takeoff, the birds accumulate and store large amounts 
of fat to fuel migration and undergo substantial changes in metabolic 
rates. In addition, leg muscles, gizzard (a muscular organ used for 
grinding food), stomach, intestines, and liver all decrease in size, 
while pectoral (chest) muscles and heart increase in size. Due to these 
physiological changes, C. canutus arriving from lengthy migrations are 
not able to feed maximally until their digestive systems regenerate, a 
process that may take several days. Because stopovers are time-
constrained, C. canutus requires stopovers rich in easily digested food 
to achieve adequate weight gain (Niles et al. 2008, pp. 28-29; van Gils 
et al. 2005a, p. 2609; van Gils et al. 2005b, pp. 126-127; Piersma et 
al. 1999, pp. 405; 412) that fuels the next migratory flight and, upon 
arrival in the Arctic, fuels a body transformation to breeding 
condition (Morrison 2006, pp. 610-612). Red knots from different 
wintering areas appear to employ different migration strategies, 
including differences in timing, routes, and stopover areas. However, 
full segregation of migration strategies, routes, or stopover areas 
does not occur among red knots from different wintering areas.
    Major spring stopover areas along the Atlantic coast include 
R[iacute]o Gallegos, Pen[iacute]nsula Vald[eacute]s, and San Antonio 
Oeste (Patagonia, Argentina); Lagoa do Peixe (eastern Brazil, State of 
Rio Grande do Sul); Maranh[atilde]o (northern Brazil); the Virginia 
barrier islands (United States); and Delaware Bay (Delaware and New 
Jersey, United States) (Cohen et al. 2009, p. 939; Niles et al. 2008, 
p. 19; Gonz[aacute]lez 2005, p. 14). Important fall stopover sites 
include southwest Hudson Bay (including the Nelson River delta), James 
Bay, the north shore of the St. Lawrence River, the Mingan Archipelago, 
and the Bay of Fundy in Canada; the coasts of Massachusetts and New 
Jersey and the mouth of the Altamaha River in Georgia, United States; 
the Caribbean (especially Puerto Rico and the Lesser Antilles); and the 
northern coast of South America from Brazil to Guyana (Newstead et al. 
in press; Niles 2012a; D. Mizrahi pers. comm. October 16, 2011; Niles 
et al. 2010a, pp. 125-136; Schneider and Winn 2010, p. 3; Niles et al. 
2008, pp. 30, 75, 94; B. Harrington pers. comm. March 31, 2006; Antas 
and Nascimento 1996, pp. 66; Morrison and Harrington 1992, p. 74; 
Spaans 1978, p. 72). (See supplemental document--Rufa Red Knot Ecology 
and Abundance--figure 3.) However, large and small groups of red knots, 
sometimes numbering in the thousands, may occur in suitable habitats 
all along the Atlantic and Gulf coasts from Argentina to Canada during 
migration (Niles et al. 2008, p. 29).
    Texas knots follow an inland flyway to and from the breeding 
grounds, using spring and fall stopovers along western Hudson Bay in 
Canada and in the northern Great Plains (Newstead et al. in press; 
Skagen et al. 1999). Stopover records from the Northern Plains are 
mainly in Canada, but small numbers of migrants have been sighted 
throughout the U.S. Great Plains States (eBird.org 2012). Some red 
knots wintering in the Southeastern United States and the Caribbean 
migrate north along the U.S. Atlantic coast before flying overland to 
central Canada from the mid-Atlantic, while others migrate overland 
directly to the Arctic from the Southeastern U.S. coast (Niles et al. 
in press). These eastern red knots typically make a short stop at James 
Bay in Canada, but may also stop briefly along the Great Lakes, perhaps 
in response to weather conditions (Niles et al. 2008, pp. 20, 24; 
Morrison and Harrington 1992, p. 79). Red knots are restricted to the 
ocean coasts during winter, and occur primarily along the coasts during 
migration. However, small numbers of rufa red knots are reported 
annually across the interior United States (i.e., greater than 25 miles 
from the Gulf or Atlantic Coasts) during spring and fall migration--
these reported sightings are concentrated along the Great Lakes, but 
multiple reports have been made from nearly every interior State 
(eBird.org 2012).
Migration and Wintering Habitat
    Long-distance migrant shorebirds are highly dependent on the 
continued existence of quality habitat at a few key staging areas. 
These areas serve as stepping stones between wintering and breeding 
areas. Conditions or factors influencing shorebird populations on 
staging areas control much of the remainder of the annual cycle and 
survival of the birds (Skagen 2006, p. 316; International Wader Study 
Group 2003, p. 10). At some stages of migration, very high proportions 
of entire populations may use a single migration staging site to 
prepare for long flights. Red knots show some fidelity to particular 
migration staging areas between years (Duerr et al. 2011, p. 16; 
Harrington 2001, pp. 8-9, 21).
    Habitats used by red knots in migration and wintering areas are 
similar in character, generally coastal marine and estuarine (partially 
enclosed tidal area where fresh and salt water mixes) habitats with 
large areas of exposed intertidal sediments. In North America, red 
knots are commonly found along sandy, gravel, or cobble beaches, tidal 
mudflats, salt marshes, shallow coastal impoundments and lagoons, and 
peat banks (Cohen et al. 2010a, pp. 355, 358-359; Cohen et al. 2009, p. 
940; Niles et al. 2008, pp. 30, 47; Harrington 2001, pp. 8-9; Truitt et 
al. 2001, p. 12). In many wintering and stopover areas, quality high-
tide roosting habitat (i.e., close to feeding areas, protected from 
predators, with sufficient space during the highest tides, free from 
excessive human disturbance) is limited (K. Kalasz pers. comm. November 
26, 2012; L. Niles pers. comm. November 19, 2012). The supra-tidal 
(above the high tide) sandy habitats of inlets provide important areas 
for roosting, especially at higher tides when intertidal habitats are 
inundated (Harrington 2008, pp. 2, 4-5).
Migration and Wintering Food
    Across all subspecies, Calidris canutus is a specialized 
molluscivore, eating hard-shelled mollusks, sometimes supplemented with 
easily accessed softer invertebrate prey, such as shrimp- and crab-like 
organisms, marine worms, and horseshoe crab (Limulus polyphemus) eggs 
(Piersma and van Gils 2011, p. 9; Harrington 2001, pp. 9-11). Mollusk 
prey are swallowed whole and crushed in the gizzard (Piersma and van 
Gils 2011, pp. 9-11). From studies of other subspecies, Zwarts and 
Blomert (1992, p. 113) concluded that C. canutus cannot ingest

[[Page 60028]]

prey with a circumference greater than 1.2 in (30 millimeters (mm)). 
Foraging activity is largely dictated by tidal conditions, as C. 
canutus rarely wade in water more than 0.8 to 1.2 in (2 to 3 cm) deep 
(Harrington 2001, p. 10). Due to bill morphology, C. canutus is limited 
to foraging on only shallow-buried prey, within the top 0.8 to 1.2 in 
(2 to 3 cm) of sediment (Gerasimov 2009, p. 227; Zwarts and Blomert 
1992, p. 113).
    The primary prey of the rufa red knot in non-breeding habitats 
include blue mussel (Mytilus edulis) spat (juveniles); Donax and Darina 
clams; snails (Littorina spp.), and other mollusks, with polycheate 
worms, insect larvae, and crustaceans also eaten in some locations. A 
prominent departure from typical prey items occurs each spring when red 
knots feed on the eggs of horseshoe crabs, particularly during the key 
migration stopover within the Delaware Bay of New Jersey and Delaware. 
Delaware Bay serves as the principal spring migration staging area for 
the red knot because of the availability of horseshoe crab eggs (Clark 
et al. 2009, p. 85; Harrington 2001, pp. 2, 7; Harrington 1996, pp. 76-
77; Morrison and Harrington 1992, pp. 76-77), which provide a 
superabundant source of easily digestible food.
    Red knots and other shorebirds that are long-distance migrants must 
take advantage of seasonally abundant food resources at intermediate 
stopovers to build up fat reserves for the next non-stop, long-distance 
flight (Clark et al. 1993, p. 694). Although foraging red knots can be 
found widely distributed in small numbers within suitable habitats 
during the migration period, birds tend to concentrate in those areas 
where abundant food resources are consistently available from year to 
    In the United States, red knot populations declined sharply in the 
late 1800s and early 1900s due to excessive sport and market hunting, 
followed by hunting restrictions and signs of population recovery by 
the mid-1900s (Urner and Storer 1949, pp. 178-183; Stone 1937, p. 465; 
Bent 1927, p. 132). However, it is unclear whether the red knot 
population fully recovered its historical numbers (Harrington 2001, p. 
22) following the period of unregulated hunting.
    More recently, long-term survey data from two key areas (Tierra del 
Fuego wintering area and Delaware Bay spring stopover site) both show a 
roughly 75 percent decline in red knot numbers since the 1980s (A. Dey 
pers. comm. October 12, 2012; G. Morrison pers. comm. August 31, 2012; 
Dey et al. 2011a, pp. 2-3; Clark et al. 2009, p. 88; Morrison et al. 
2004, p. 65; Morrison and Ross 1989, Vol. 2, pp. 226, 252; Kochenberger 
1983, p. 1; Dunne et al. 1982, p. 67; Wander and Dunne, 1982, p. 60). 
Survey data for the Virginia barrier islands spring stopover area show 
no trend since 1995 (B. Watts pers. comm. November 15, 2012). Survey 
data are also available for the Brazil, Northwest Gulf of Mexico, and 
Southeast-Caribbean wintering areas, but are insufficient to infer 

Climate Change

    Comprehensive background information regarding climate change is 
available as a supplemental document (``Climate Change Background'') on 
the Internet at http://www.regulations.gov (Docket No. FWS-R5-ES-2013-
0097; see ADDRESSES section for further access instructions). As 
explained in the supplemental document, the International Panel on 
Climate Change (IPCC) uses standardized terms to define levels of 
confidence (from ``very high'' to ``very low'') and likelihood (from 
``virtually certain'' to ``exceptionally unlikely''). When used in this 
context, these terms are given in quotes in this document.

Summary of Factors Affecting the Species

    Section 4 of the Act (16 U.S.C. 1533), and its implementing 
regulations at 50 CFR part 424, set forth the procedures for adding 
species to the Federal Lists of Endangered and Threatened Wildlife and 
Plants. Under section 4(a)(1) of the Act, we may list a species based 
on any of the following five factors: (A) The present or threatened 
destruction, modification, or curtailment of its habitat or range; (B) 
overutilization for commercial, recreational, scientific, or 
educational purposes; (C) disease or predation; (D) the inadequacy of 
existing regulatory mechanisms; and (E) other natural or manmade 
factors affecting its continued existence. Listing actions may be 
warranted based on any of the above threat factors, singly or in 
combination. Each of these factors is discussed below.

Overview of Threats Related to Climate Change

    We discuss the ongoing and projected effects of climate change, and 
the levels of certainty associated with these effects, in the 
appropriate sections of the five-factor analysis. For example, habitat 
loss from sea level rise is discussed under Factor A, and asynchronies 
(``mismatches'') in the timing of the annual cycle are discussed under 
Factor E. Here we present an overview of threats stemming from climate 
change, which are addressed in more detail in the sections that follow.
    The natural history of Arctic-breeding shorebirds makes this group 
of species particularly vulnerable to global climate change (e.g., 
Meltofte et al. 2007, entire; Piersma and Lindstr[ouml]m 2004, entire; 
Rehfisch and Crick 2003, entire; Piersma and Baker 2000, entire; 
Z[ouml]ckler and Lysenko 2000, entire; Lindstr[ouml]m and Agrell 1999, 
entire). Relatively low genetic diversity, which is thought to be a 
consequence of survival through past climate-driven population 
bottlenecks, may put shorebirds at more risk from human-induced climate 
variation than other avian taxa (Meltofte et al. 2007, p. 7); low 
genetic diversity may result in reduced adaptive capacity as well as 
increased risks when population sizes drop to low levels.
    In the short term, red knots may benefit if warmer temperatures 
result in fewer years of delayed horseshoe crab spawning in Delaware 
Bay (Smith and Michaels 2006, pp. 487-488) or fewer occurrences of late 
snow melt in the breeding grounds (Meltofte et al. 2007, p. 7). 
However, there are indications that changes in the abundance and 
quality of red knot prey are already under way (Escudero et al. 2012, 
pp. 359-362; Jones et al. 2010, pp. 2255-2256), and prey species face 
ongoing climate-related threats from warmer temperatures (Jones et al. 
2010, pp. 2255-2256; Philippart et al. 2003 p. 2171; Rehfisch and Crick 
2003, p. 88), ocean acidification (National Research Council (NRC) 
2010, p. 286; Fabry et al. 2008, p. 420), and possibly increased 
prevalence of disease and parasites (Ward and Lafferty 2004, p. 543). 
In addition, red knots face imminent threats from loss of habitat 
caused by sea level rise (NRC 2010, p. 44; Galbraith et al. 2002, pp. 
177-178; Titus 1990, p. 66), and increasing asynchronies 
(``mismatches'') between the timing of their annual breeding, 
migration, and wintering cycles and the windows of peak food 
availability on which the birds depend (Smith et al. 2011a, pp. 575, 
581; McGowan et al. 2011a, p. 2; Meltofte et al. 2007, p. 36; van Gils 
et al. 2005a, p. 2615; Baker et al. 2004, p. 878).
    Several threats are related to the possibility of changing storm 
patterns. While variation in weather is a natural occurrence and is 
normally not considered a threat to the survival of a species, 
persistent changes in the frequency, intensity, or timing of storms at 
key locations where red knots congregate (e.g., key stopover areas) can 
pose a threat (see Factor E and the ``Coastal Storms and Extreme 

[[Page 60029]]

section of the Climate Change Background supplemental document). Storms 
impact migratory shorebirds like the red knot both directly and 
indirectly. Direct impacts include energetic costs from a longer 
migration route as birds avoid storms, blowing birds off course, and 
outright mortality (Niles et al. 2010a, p. 129). Indirect impacts 
include changes to habitat suitability, storm-induced asynchronies 
between migration stopover periods and the times of peak prey 
availability, and possible prompting of birds to take refuge in areas 
where shorebird hunting is still practiced (Niles et al. 2012, p. 1; 
Dey et al. 2011b, pp. 1-2; Nebel 2011, p. 217).
    With arctic warming, vegetation conditions in the red knot's 
breeding grounds are expected to change, causing the zone of nesting 
habitat to shift and perhaps contract, but this process may take 
decades to unfold (Feng et al. 2012, p. 1366; Meltofte et al. 2007, p. 
36; Kaplan et al. 2003, p. 10). Ecological shifts in the Arctic may 
appear sooner. High uncertainty exists about when and how changing 
interactions among vegetation, predators, competitors, prey, parasites, 
and pathogens may affect the red knot, but the impacts are potentially 
profound (Fraser et al. 2013; entire; Schmidt et al. 2012, p. 4421; 
Meltofte et al. 2007, p. 35; Ims and Fuglei 2005, entire).
    In summary, climate change is expected to affect red knot fitness 
and, therefore, survival through direct and indirect effects on 
breeding and nonbreeding habitat, food availability, and timing of the 
birds' annual cycle. Ecosystem changes in the arctic (e.g., changes in 
predation patterns and pressures) may also reduce reproductive output. 
Together, these anticipated changes will likely negatively influence 
the long-term survival of the rufa red knot.
Factor A. The Present or Threatened Destruction, Modification, or 
Curtailment of Its Habitat or Range
    In this section, we present and assess the best available 
scientific and commercial data regarding ongoing threats to the 
quantity and quality of red knot habitat. Within the nonbreeding 
portion of the range, red knot habitat is primarily threatened by the 
highly interrelated effects of sea level rise, shoreline stabilization, 
and coastal development. Lesser threats to nonbreeding habitat include 
agriculture and aquaculture, invasive vegetation, and beach maintenance 
activities. Within the breeding portion of the range, the primary 
threat to red knot habitat is from climate change. With arctic warming, 
vegetation conditions in the breeding grounds are expected to change, 
causing the zone of nesting habitat to shift and perhaps contract. 
Arctic freshwater systems--foraging areas for red knots during the 
nesting season--are particularly sensitive to climate change.
Factor A--Accelerating Sea Level Rise
    For most of the year, red knots live in or immediately adjacent to 
intertidal areas. These habitats are naturally dynamic, as shorelines 
are continually reshaped by tides, currents, wind, and storms. Coastal 
habitats are susceptible to both abrupt (storm-related) and long-term 
(sea level rise) changes. Outside of the breeding grounds, red knots 
rely entirely on these coastal areas to fulfill their roosting and 
foraging needs, making the birds vulnerable to the effects of habitat 
loss from rising sea levels. Because conditions in coastal habitats are 
also critical for building up nutrient and energy stores for the long 
migration to the breeding grounds, sea level rise affecting conditions 
on staging areas also has the potential to impact the red knot's 
ability to breed successfully in the Arctic (Meltofte et al. 2007, p. 
    According to the National Research Council (NRC) (2010, p. 43), the 
rate of global sea level rise has increased from about 0.02 in (0.6 mm) 
per year in the late 19th century to approximately 0.07 in (1.8 mm) per 
year in the last half of the 20th century. The rate of increase has 
accelerated, and over the past 15 years has been in excess of 0.12 in 
(3 mm) per year. In 2007, the IPCC estimated that sea level would 
``likely'' rise by an additional 0.6 to 1.9 feet (ft) (0.18 to 0.59 
meters (m)) by 2100 (NRC 2010, p. 44). This projection was based 
largely on the observed rates of change in ice sheets and projected 
future thermal expansion of the oceans but did not include the 
possibility of changes in ice sheet dynamics (e.g., rates and patterns 
of ice sheet growth versus loss). Scientists are working to improve how 
ice dynamics can be resolved in climate models. Recent research 
suggests that sea levels could potentially rise another 2.5 to 6.5 ft 
(0.8 to 2 m) by 2100, which is several times larger than the 2007 IPCC 
estimates (NRC 2010, p. 44; Pfeffer et al. 2008, p. 1340). However, 
projected rates of sea level rise estimates remain rather uncertain, 
due mainly to limits in scientific understanding of glacier and ice 
sheet dynamics (NRC 2010, p. 44; Pfeffer et al. 2008, p. 1342).
    The amount of sea level change varies regionally because of 
different rates of settling (subsidence) or uplift of the land, and 
because of differences in ocean circulation (NRC 2010, p. 43). In the 
last century, for example, sea level rise along the U.S. mid-Atlantic 
and Gulf coasts exceeded the global average by 5 to 6 in (13 to 15 cm) 
because coastal lands in these areas are subsiding (U.S. Environmental 
Protection Agency (USEPA) 2013). Land subsidence also occurs in some 
areas of the Northeast, at current rates of 0.02 to 0.04 in (0.5 to 1 
mm) per year across this region (Ashton et al. 2007, pp. 5-6), 
primarily the result of slow, natural geologic processes (National 
Oceanic and Atmospheric Administration (NOAA) 2013b, p. 28). Due to 
regional differences, a 2-ft (0.6-m) rise in global sea level by the 
end of this century would result in a relative sea level rise of 2.3 ft 
(0.7 m) at New York City, 2.9 ft (0.9 m) at Hampton Roads, Virginia, 
and 3.5 ft (1.1 m) at Galveston, Texas (U.S. Global Change Research 
Program (USGCRP) 2009, p. 37). Table 1 shows that local rates of sea 
level rise in the range of the red knot over the second half of the 
20th century were generally higher than the global rate of 0.07 in (1.8 
mm) per year.

  Table 1--Local Sea Level Trends From Within the Range of the Red Knot
                              [NOAA 2012a]
                                      Mean local sea
              Station                level trend  (mm     Data period
                                        per year)
Pointe-Au-P[egrave]re, Canada.....       -0.36  0.40
Woods Hole, Massachusetts.........  2.61           1932-2006
Cape May, New Jersey..............  4.06           1965-2006
Lewes, Delaware...................  3.20           1919-2006
Chesapeake Bay Bridge Tunnel,       6.05           1975-2006
 Virginia.........................               1.14

[[Page 60030]]

Beaufort, North Carolina..........  2.57           1953-2006
Clearwater Beach, Florida.........  2.43           1973-2006
Padre Island, Texas...............  3.48           1958-2006
Punto Deseado, Argentina..........       -0.06  1.93

    Data from along the U.S. Atlantic coast suggest a relationship 
between rates of sea level rise and long-term erosion rates; thus, 
long-term coastal erosion rates may increase as sea level rises 
(Florida Oceans and Coastal Council 2010, p. 6). However, even if such 
a correlation is borne out, predicting the effect of sea level rise on 
beaches is more complex. Even if wetland or upland coastal lands are 
lost, sandy or muddy intertidal habitats can often migrate or reform. 
However, forecasting how such changes may unfold is complex and 
uncertain. Potential effects of sea level rise on beaches vary 
regionally due to subsidence or uplift of the land, as well as the 
geological character of the coast and nearshore (U.S. Climate Change 
Science Program (CCSP) 2009b, p. XIV; Galbraith et al. 2002, p. 174). 
Precisely forecasting the effects of sea level rise on particular 
coastal habitats will require integration of diverse information on 
local rates of sea level rise, tidal ranges, subsurface and coastal 
topography, sediment accretion rates, coastal processes, and other 
factors that is beyond the capability of current models (CCSP 2009b, 
pp. 27-28; Frumhoff et al. 2007, p. 29; Thieler and Hammar-Klose 2000; 
Thieler and Hammar-Klose 1999). Furthermore, human manipulation of the 
coastal environment through beach nourishment, hard stabilization 
structures, and coastal development may negate forecasts based only on 
the physical sciences (Thieler and Hammar-Klose 2000; Thieler and 
Hammar-Klose 1999). Available information on the effects of sea level 
rise varies in specificity across the range of the red knot. At the 
international scale, only a relatively coarse assessment is possible. 
At the national scale, the U.S. Geological Survey's (USGS) Coastal 
Vulnerability Index (CVI) provides information at an intermediate level 
of resolution (Thieler and Hammar-Klose 2000; Thieler and Hammar-Klose 
1999). Finally, more detailed regional, state, and local information is 
available for certain red knot wintering or stopover areas.
Sea Level Rise--International
    We conducted an analysis to consider the possible effects of a 3.3-
ft (1-m) increase in sea level in important nonbreeding habitats 
outside the United States, using global topographic mapping from the 
University of Arizona (Arizona Board of Regents, 2012; J. Weiss pers. 
comm. November 13, 2012; Weiss et al. 2011, p. 637). This visualization 
tool incorporates only current topography at a horizontal resolution of 
0.6 mi (1 km) (Arizona Board of Regents, 2012). We did not evaluate 
Canadian breeding habitats for sea level rise because red knots nest 
inland above sea level (at elevations of up to 492 ft (150 m)) and, 
while in the Arctic, knots forage in freshwater wetlands and rarely 
contact salt water (Burger et al. 2012a, p. 26; Niles et al. 2008, pp. 
27, 61).
    We selected a 3.3-ft (1-m) sea level increase based on the 
availability of a global dataset, and because it falls within the 
current range of 2.6 to 6.6 ft (0.8 to 2 m) projected by 2100 (NRC 
2010, p. 44). Along with topography (e.g., land elevation relative to 
sea level), the local tidal regime is an important factor in attempting 
to forecast the likely effects of sea level rise (Strauss et al. 2012, 
pp. 2, 6-8). Therefore, we also considered local tidal ranges (the 
vertical distance between the high tide and the succeeding low tide) 
and other factors that may influence the extent or effects of sea level 
rise when site-specific information was available and appropriate. In 
the 1990s, some studies (e.g., Gornitz et al. 1994, p. 330) classified 
coastlines with a large tidal range (``macrotidal'') (i.e., with a 
tidal range greater than 13 ft (4 m)) as more vulnerable to sea level 
rise because a large tidal range is associated with strong tidal 
currents that influence coastal behavior (Thieler and Hammar-Klose 
2000; Thieler and Hammar-Klose 1999). More recently, however, the USGS 
inverted this ranking such that a macrotidal coastline is classified as 
low vulnerability. This change was based primarily on the potential 
influence of storms on coastal evolution, and the impact of storms 
relative to the tidal range. For example, on a tidal coastline, there 
is only a 50 percent chance of a storm occurring at high tide. Thus, 
for a region with a 13.1-ft (4-m) tidal range, a storm having a 9.8-ft 
(3-m) surge height is still up to 3.3 ft (1 m) below the elevation of 
high tide for half of the duration of each tidal cycle. A microtidal 
coastline (with a tidal range less than 6.6 ft (2 m)), on the other 
hand, is essentially always ``near'' high tide and, therefore, always 
at the greatest risk of significant storm impact (Thieler and Hammar-
Klose 2000; Thieler and Hammar-Klose 1999).
    Notwithstanding uncertainty about how tidal range will influence 
overall effects of sea level rise on coastal change, tidal range is 
also important due to the red knot's dependence on intertidal areas for 
foraging habitat. Along macrotidal coasts, large areas of intertidal 
habitat are exposed during low tide. In such areas, some intertidal 
habitat is likely to remain even with sea level rise, whereas a greater 
proportion of intertidal habitats may become permanently inundated in 
areas with smaller tidal ranges.
    Although no local modeling is available, large tidal ranges in the 
southernmost red knot wintering areas suggest extensive tidal flats 
will persist, although a projected 3.3-ft (1-m) rise in sea level will 
likely result in some habitat loss. Despite decreases in recent 
decades, Bah[iacute]a Lomas in the Chile portion of Tierra del Fuego is 
still the largest single red knot wintering site. Extensive intertidal 
flats at Bah[iacute]a Lomas are the result of daily tidal variation on 
the order of 20 to 30 ft (6 to 9 m), depending on the season. The 
Bah[iacute]a Lomas flats extend for about 30 mi (50 km) along the 
coast, and during spring tides the intertidal distance reaches 4.3 mi 
(7 km) in places (Niles et al. 2008, p. 50). Some lands in the eastern 
portion of Bah[iacute]a Lomas would potentially be impacted by a 3.3-ft 
(1-m) rise in sea level but not lands in the western portion. In the 
Argentina portion of

[[Page 60031]]

Tierra del Fuego, red knots winter chiefly in Bah[iacute]a San 
Sebasti[aacute]n and R[iacute]o Grande (Niles et al. 2008, p. 17). 
Tides in Bah[iacute]a San Sebasti[aacute]n are up to 13 ft (4 m). Tides 
in R[iacute]o Grande average 18 ft (5.5 m), with a maximum of 27.6 ft 
(8.4 m) (Escudero et al. 2012, p. 356). At high tides, some lands 
throughout Bah[iacute]a San Sebasti[aacute]n and R[iacute]o Grande 
would potentially be impacted by a 3.3-ft (1-m) rise in sea level; red 
knot habitat could be reduced at these sites.
    On the Patagonian coast of Argentina, key red knot wintering and 
stopover areas include the R[iacute]o Gallegos estuary and Bah[iacute]a 
de San Antonio (San Antonio Oeste) (Niles et al. 2008, p. 19). Tides at 
R[iacute]o Gallegos can rise 29 ft (8.8 m) (NOAA 2013c), and low tide 
exposes extensive intertidal silt-clay flats that in some places extend 
out for 0.9 mi (1.5 km) (Western Hemisphere Shorebird Reserve Network 
(WHSRN) 2012). With a 3.3-ft (1-m) sea level rise, extensive areas on 
the north side of the R[iacute]o Gallegos estuary, west of the City of 
R[iacute]o Gallegos, would potentially be impacted. At Bah[iacute]a de 
San Antonio, the tidal range is 30.5 ft (9.3 m), and at low tide the 
water can withdraw as far as 4.3 mi (7 km) from the coastal dunes. 
Extensive tidal flats will persist at the lower tidal levels, even with 
a projected 3.3-ft (1-m) rise in sea level.
    Despite decreases in recent decades, Lagoa do Peixe is a key spring 
stopover site for red knots on the east coast of Brazil. The lagoon is 
connected to the Atlantic Ocean through wind action and rain and 
sometimes through pumping or an artificial inlet (WHSRN 2012; Niles et 
al. 2008, p. 48). The shallow waters and mudflats that support foraging 
red knots are exposed irregularly by wind action and rain. The Atlantic 
coastline fronting Lagoa do Peixe would be impacted by a 3.3-ft (1-m) 
rise in sea level, which could potentially result in more extensive 
inundation of the lagoon through the inlet or via storm surges.
    Coastal areas in North-Central Brazil in the State of 
Maranh[atilde]o are used by migrating and wintering red knots, which 
forage on sandy beaches and mudflats and use extensive areas of 
mangroves (Niles et al. 2008, p. 48). In this region, local tidal 
ranges of up to 32.8 ft (10 m) are associated with strong tidal 
currents (Muehe 2010, p. 177). The largest concentrations of red knots 
have been recorded along the islands and complex coastline just east of 
Turia[ccedil][uacute] Bay (Niles et al. 2008, pp. 71, 153), which has a 
tidal range of up to 26.2 ft (8 m) (Rebelo-Mochel and Ponzoni 2007, p. 
684). Despite the large tidal ranges, topographic mapping suggests that 
nearly all the low-lying islands and coastline now used by red knots 
could become inundated by a 3.3-ft (1-m) sea level rise. As this region 
has low human population density (Rebelo-Mochel and Ponzoni 2007, p. 
684), landward migration of suitable red knot habitats may be possible 
as sea levels rise. Muehe (2010, p. 177) suggested that the mangroves 
might be able to compensate for rising sea levels by migrating landward 
and laterally in some places, but movement could be frequently limited 
by the presence of cliffs along the open coasts and estuaries. Mangrove 
adaptation may not be sustained at rates of sea level rise higher than 
0.3 in (7 mm) per year (Muehe 2010, p. 177), as would occur under the 
3.3-ft (1-m) sea level rise scenario (CCSP 2009b, p. XV).
    The IPCC (2007c, p. 58) evaluated the effects of a 1.6-ft (0.5-m) 
rise in sea level on small Caribbean islands, and found that up to 38 
percent (24 percent standard deviation) of the total 
current beach could be lost, with lower, narrower beaches being the 
most vulnerable. The IPCC did not relate this beach loss to shorebirds, 
but did find that sea turtle nesting habitat (the basic characteristics 
of which are similar to, and which often overlaps with, shorebird 
habitat) would be reduced by one-third under this 1.6-ft (0.5-m) 
scenario, which is now considered a low estimate of the sea level rise 
that is likely to occur by 2100 (NRC 2010, p. 44). In the Bahamas, 
ocean acidification (discussed further under Factor E, below) may 
exacerbate the effects of sea level rise by interfering with the biotic 
and chemical formation of carbonate-based sediments (Hallock 2005, pp. 
25-27; Feely et al. 2004, pp. 365-366).
    In Canada, the islands of the Mingan Archipelago could be inundated 
by a 3.3-ft (1-m) sea level rise. The topographic mapping shows some 
inundation of the adjacent mainland coastline (Mingan Archipelago 
National Park), as well as the Nelson River delta and the shores of 
James Bay, but, except where blocked by topography, red knot habitat in 
these areas may have more potential to migrate than on the islands. 
With a 3.3-ft (1-m) sea level rise, little intertidal area would be 
lost in the Bay of Fundy, which has the greatest tidal ranges in the 
world (up to 38.4 ft (11.7 m)) (NOAA 2013c), although some habitats 
around the mouths of rivers may become inundated. These areas are 
important stopover sites for red knots during migration (Newstead et 
al. in press; Niles et al. 2010a, pp. 125-136; Niles et al. 2008, p. 
    Based on our analysis of topography, tidal range, and other 
factors, some habitat loss in Tierra del Fuego is expected with a 3.3-
ft (1-m) rise in sea level, but considerable foraging habitat is likely 
to remain due to very large tidal ranges. Several key South American 
and Canadian stopover sites we examined are likely to be affected by 
sea level rise. In both Canada and South America, red knot coastal 
habitats are expected to migrate inland under a mid-range estimate 
(3.3-ft; 1-m) of sea level rise, except where constrained by 
topography, coastal development, or shoreline stabilization structures. 
The north coast of Brazil, low-lying Caribbean beaches, and Canada's 
Mingan Islands Archipelago may be exceptions and may experience more 
substantial red knot habitat loss even under moderate sea level rise. 
The upper range (6.6 ft; 2 m) of current predictions was not evaluated 
but would be expected to exceed the migration capacity of many more red 
knot habitats than the 3.3-ft (1-m) scenario. Thus, sea level rise is 
expected to result in localized habitat loss at several non-U.S. 
wintering and stopover areas. Cumulatively, these losses could affect 
the ability of red knots to complete their annual cycles that in turn 
may possibly affect fitness and survival.
Sea Level Rise--United States
United States--Mechanisms of Habitat Loss
    Comparing topography to best available scenarios of sea level rise 
provides an estimate of the land area that may be vulnerable to the 
effects of sea level rise, but does not incorporate regional variation 
in tidal regimes (Strauss et al. 2012, p. 2), coastal processes (e.g., 
barrier island migration), or environmental changes that may occur as 
sea level rises (e.g., salt marsh deterioration) (CCSP 2009b, p. 44). 
Because the majority of the Atlantic and Gulf coasts consist of sandy 
shores, inundation alone is unlikely to reflect the potential 
consequences of sea level rise. Instead, long-term shoreline changes 
will involve contributions from both inundation and erosion, as well as 
changes to other coastal environments such as wetland losses. Most 
portions of the open coast of the United States will be subject to 
significant physical changes and erosion over the next century because 
the majority of coastlines consist of sandy beaches, which are highly 
mobile and in a state of continual change (CCSP 2009b, p. 44).
    By altering coastal geomorphology, sea level rise will cause 
significant and often dramatic changes to coastal landforms including 
barrier islands,

[[Page 60032]]

beaches, and intertidal flats (CCSP 2009b, p. 13; Rehfisch and Crick 
2003, p. 89), primary red knot habitats. Due to increasing sea levels, 
storm-surge-driven floods now qualifying as 100-year events are 
projected to occur as often as every 10 to 20 years along most of the 
U.S. Atlantic coast by 2050, with even higher frequencies of such large 
floods in certain localized areas (Tebaldi et al. 2012, pp. 7-8). 
Rising sea level not only increases the likelihood of coastal flooding, 
but also changes the template for waves and tides to sculpt the coast, 
which can lead to loss of land orders of magnitude greater than that 
from direct inundation alone (Ashton et al. 2007, p. 1). Although 
scientists agree that the predicted sea level rise will result in 
severe beach erosion and shoreline retreat through the next century, 
quantitative predictions of these changes are uncertain, hampered by 
limited understanding of coastal responses and the innate complexity of 
the coastal zone (Ashton et al. 2007, p. 9). Coastal responses to 
climate change will not likely be homogeneous along the coast, due to 
local differences in geology and other factors (Ashton et al. 2007, p. 
    Beach losses accumulate over time, mostly during infrequent, high-
energy events, both seasonal events and rare extreme storms (Ashton et 
al. 2009, p. 7). Even the long-term coastal response to sea level rise 
depends on the magnitudes and timing of stochastically unpredictable 
future storm events (Ashton et al. 2009, p. 9). Most erosion events on 
the Atlantic and Gulf coasts are the result of storms. With sea level 
rise, increased erosion is caused by longer storm surges and greater 
wave action from both tropical (especially on the southeast Atlantic 
and Gulf coasts) and extra-tropical storms (Higgins 2008, p. 49). The 
Atlantic and Gulf coast shorelines are especially vulnerable to long-
term sea level rise, as well as any increase in the frequency of storm 
surges or hurricanes. The slope of these areas is so gentle that a 
small rise in sea level produces a large inland shift of the shoreline 
(Higgins 2008, p. 49). As discussed in the supplemental document 
Climate Change Background, increased magnitude and changing geographic 
distributions of coastal storms are predicted, but projections about 
changing storm patterns are associated with only ``low to medium 
confidence'' levels (IPCC 2012, p. 13).
    In addition to the effects of storm surges, red knot habitats could 
also be affected by the increasing frequency and intensity of extreme 
precipitation events (see supplemental document--Climate Change 
Background). Since the ecological dynamics of sandy beaches can be 
linked to freshwater discharge from rivers, global changes in land-
ocean coupling via freshwater outflows are predicted to affect the 
ecology of beaches (Schlacher et al. 2008a, p. 84). For example, 
persistent increases in freshwater discharges could cause localized 
habitat changes by allowing invasive or incompatible vegetation to 
become established, changing the seed distribution of native grasses, 
or altering salinity (F. Weaver pers. comm. April 17, 2013) (also see 
Factor E--Reduced Food Availability--Other Aspects of Climate Change).
    Red knot migration and wintering habitats in the United States 
generally consist of sandy beaches that are dynamic and subject to 
seasonal erosion and accretion (the accumulation of sediment). Sea 
level rise and shoreline erosion have reduced availability of 
intertidal habitat used for red knot foraging, and in some areas, 
roosting sites have also been affected (Niles et al. 2008, p. 97). With 
moderately rising sea levels, red knot habitats in many portions of the 
United States would be expected to migrate or reform rather than be 
lost, except where they are constrained by coastal development or 
shoreline stabilization (Titus et al. 2009, p. 1) (discussed in 
subsequent sections). However, if the sea rises more rapidly than the 
rate with which a particular coastal system can keep pace, it could 
fundamentally change the state of the coast (CCSP 2009b, p. 2). The 
upper range (6.6 ft; 2 m) of current sea level rise predictions would 
be expected to exceed the migration capacity of many more red knot 
areas than the 3.3-ft (1-m) scenario.
Mechanisms--Estuarine Beaches
    As sea level rises, the fate of estuarine beaches (e.g., along 
Delaware Bay) depends on their ability to migrate and the availability 
of sediment to replenish eroded sands. Estuarine beaches continually 
erode, but under natural conditions the landward and waterward 
boundaries usually retreat by about the same distance. Shoreline 
protection structures may prevent migration, effectively squeezing 
beaches between development and the water (CCSP 2009b, p. 81).
Mechanisms--Barrier Island Beaches
    The barrier islands of the Atlantic and Gulf coasts have evolved in 
the context of modest and decelerating sea level rise over the past 
5,000 years. If human activities do not interfere, these barrier 
systems can typically remain intact as they migrate landward, given sea 
level rise rates typical of those of the last few millennia (CCSP 
2009b, p. 186; Ashton et al. 2007, p. 2). Without stabilization, many 
low-lying, undeveloped islands will migrate toward the mainland, pushed 
by the overwashing of sand eroding from the seaward side that gets re-
deposited in the bay (Scavia et al. 2002, p. 152). However, even 
without human intervention, some barrier islands may respond to sea 
level rise by breaking up and drowning in place, rather than migrating 
(Titus 1990, p. 67). Coastal geologists are not yet able to forecast 
whether a particular island will migrate or break up, although island 
disintegration appears to be more frequent in areas with high rates of 
relative sea level rise (Titus 1990, p. 67); thus, disintegration may 
occur more often as rates of sea level rise accelerate.
    Whether the barrier systems can continue to evolve with accelerated 
sea level rise is not clear, particularly as human intervention often 
does not permit the islands to continue to freely move landward (Ashton 
et al. 2007, p. 2). Sea level rise of 3.3 ft (1 m) may cause many 
narrow barrier islands to disintegrate (USEPA 2012). Because the 
coastal marshes behind many barrier islands become increasingly 
inundated, sufficiently high rates of sea level rise could result in 
threshold behaviors that produce wholesale reorganizations of entire 
barrier systems (CCSP 2009b, p. 2; Ashton et al. 2007, p. 10). Crossing 
threshold levels of interaction between coastal elevation, sea level, 
and storm-driven surges and waves can result in dramatic changes in 
coastal topography, including the loss of some low-lying islands 
(Florida Oceans and Coastal Council 2010, p. 7; CCSP 2009b, p. 50; 
Lavoie 2009, p. 37).
United States--Coastal Vulnerability Index
    At the national scale, the USGS CVI combines the coastal system's 
susceptibility to change with its natural ability to adapt to changing 
environmental conditions. The output is a relative measure of the 
system's natural vulnerability to the effects of sea level rise. 
Classification of vulnerability (very high, high, moderate, or low) is 
based on variables such as coastal geomorphology, regional coastal 
slope, rate of sea level rise, wave and tide characteristics, and 
historical shoreline change rates. The combination of these variables 
and the association of these variables to each other furnishes a broad 
overview of regions where physical changes are likely to occur due to 
sea level rise (Thieler and Hammar-Klose 2000; Thieler and Hammar-Klose 
    We conducted a Geographic Information System (GIS) analysis to

[[Page 60033]]

overlay the CVI mapping with important red knot habitats, which were 
delineated using data from the International Shorebird Survey 
(eBird.org 2012) and other sources. By length, about half of the 
coastline within important red knot habitats is in the ``very high'' 
vulnerability category, and about two-thirds is either ``very high'' or 
``high'' (table 2). Comparing these percentages to the Atlantic and 
Gulf coasts as a whole (less than one-third ``very high,'' only about 
half ``high'' or ``very high'') suggests that important red knot 
habitats tend to occur along higher-vulnerability portions of the 
shoreline. Red knot habitats along the Atlantic coast of New Jersey, 
Virginia, and the Carolinas and along the Gulf coast west of Florida 
are at particular risk from sea level rise. The GIS analysis does not 
reflect the potential for red knot habitats to migrate or reform (which 
is poorly known under high and accelerating rates of sea level rise) 
and did not consider human interference with coastal processes (which 
is discussed in subsequent sections).

  Table 2--Percent of Coastline (by Length) in Each Coastal Vulnerability Category; Important Red Knot Habitats
                                             Versus the Entire Coast
                                                     Very high         High          Moderate           Low
                                           Important Red Knot Habitats
Massachusetts...................................               0              10              23              67
New York........................................               0               7              50              43
New Jersey--Atlantic............................              69              10              22               0
New Jersey--Delaware Bay........................               0              77              14               9
Delaware........................................               0              37               0              63
Virginia........................................              99               1               0               0
North Carolina..................................              59              15              25               1
South Carolina..................................              59              23              18               0
Georgia.........................................              29              35              27               8
Florida--Atlantic...............................               8               7              79               6
Florida--Gulf...................................               2              41              53               3
Mississippi.....................................             100               0               0               0
Louisiana.......................................             100               0               0               0
Texas...........................................              63              20              17               0
All States combined.............................              49              21              23               7
                                                 Entire Coast *
Atlantic coast..................................              27              22              23              28
Gulf coast......................................              42              13              37               8
Atlantic and Gulf coasts combined...............              31              19              26              23
* Thieler and Hammar-Klose 2000; Thieler and Hammar-Klose 1999.

United States--Northeast and Mid-Atlantic
    In the Northeast (Maine to New Jersey), the areas most vulnerable 
to increasing shoreline erosion with sea level rise include portions of 
Cape Cod, Massachusetts; Long Island, New York; and most of coastal New 
Jersey (Cooper et al. 2008, p. 488; Frumhoff et al. 2007, p. 15). 
Because of the erosive impact of waves, especially storm waves, the 
extent of shoreline retreat and wetland loss in the Northeast is 
projected to be many times greater than the loss of land caused by the 
rise in sea level itself (Frumhoff et al. 2007, p. 15). Along the ocean 
shores of the mid-Atlantic (New York to North Carolina), which are 
composed of headlands, barrier islands, and spits, it is ``virtually 
certain'' that erosion will dominate changes in shoreline as a 
consequence of sea level rise and storms over the next century. It is 
``very likely'' that coastal landforms will undergo large changes under 
regional sea level rise scenarios of 1.6 to 3.6 ft (0.5 to 1.1 m) (CCSP 
2009b, pp. XV, 43). The response will vary locally and could be more 
variable than the changes observed over the last century. Under these 
scenarios, it is ``very likely'' that some barrier island coasts will 
cross a threshold and undergo significant changes. These changes 
include more rapid landward migration or segmentation of some barrier 
islands (CCSP 2009b, p. 43) that are likely to cause substantial 
changes to red knot habitats.
Mid-Atlantic--Delaware Bay Shorebird Habitat
    The rate of sea level rise in the Delaware Bay over the past 
century was about 0.12 in (3 mm) per year (table 1; Kraft et al. 1992, 
p. 233; Phillips 1986a, p. 430), resulting in erosion of the bay's 
shorelines and a landward extension of the inland edge of the marshes. 
For the period 1940 to 1978, Phillips (1986a, pp. 428-429) documented a 
mean erosion rate of 10.5 ft (3.2 m) per year (standard deviation of 6 
ft (1.85 m) per year) for a 32.3-mi (52-km) long section of the 
Delaware Bay shoreline in Cumberland County, New Jersey. This is a high 
rate of erosion compared to other estuaries and is affected by some 
very high local values (e.g., peninsular points, creek mouths) 
approaching 49 ft (15 m) per year (Phillips 1986a, pp. 429-430). The 
spatial pattern of the erosion was complex, with differential erosion 
resistance related to local differences in shoreline morphology 
(Phillips 1986b, pp. 57-58). Phillips's shoreline erosion studies 
(1986a, pp. 431-435; 1986b, pp. 56-60) suggested that bay-edge erosion 
was occurring more rapidly than the landward-upward extension of the 
coastal wetlands and that this pattern was likely to persist. Similar 
to the complex and heterogeneous pattern found by Phillips, Kraft et 
al. (1992, p. 233) found that some bayshore areas in Delaware were 
undergoing inundation while other areas were accreting faster than the 
local rate of sea level rise. Accompanying these sedimentary processes 
were coastal erosion rates up to 22.6 ft (6.9 m) per year along the 
Delaware portion of the bayshore (Kraft et al. 1992, p. 233). Erosion 
has led to loss of red knot roosting sites, which are already limited, 
especially around the

[[Page 60034]]

Mispillion Harbor portion of Delaware Bay (Niles et al. 2008, p. 97).
    Glick et al. (2008, p. 31) found that existing marsh along Delaware 
Bay is predicted to be inundated with greater frequency as sea level 
rises. Under 2.3 and 3.3 ft (0.7 and 1 m) of sea level rise, 43 and 77 
percent of marshes, respectively, are predicted to be lost. The area of 
estuarine beach is predicted to increase substantially, roughly 
doubling under all sea level rise scenarios. However, this finding 
assumes no additional shoreline armoring would take place. Further 
armoring may be likely, considering 6 to 8 percent of developed and 
undeveloped dry land is predicted to be lost under the various 
scenarios evaluated. At the high end (6.6-ft (2-m) sea level rise), 18 
percent of developed land would be inundated without further armoring 
(Glick et al. 2008, p. 31).
    Galbraith et al. (2002, pp. 177-178) examined several different 
scenarios of future sea level rise and projected major losses of 
intertidal habitat in Delaware Bay. Under a scenario of 1.1 ft (34 cm) 
global sea level rise, Delaware Bay was predicted to lose at least 20 
percent of its intertidal shorebird feeding habitats by 2050, and at 
least 57 percent by 2100. Under a scenario of 2.5 ft (77 cm) global sea 
level rise, Delaware Bay would lose 43 percent of its tidal flats by 
2050, but may actually see an increase of nearly 20 percent over 
baseline levels by 2100, as the coastline migrates farther inland and 
dry land is converted to intertidal (Galbraith et al. 2002, pp. 177-
178). The net increase would be realized only after a long period (50 
years) of severely reduced habitat availability, and assumes that 
landward migration would not be halted by development or armoring. Sea 
Level Affecting Marsh Modeling (SLAMM) of a 3.3-ft (1-m) sea level rise 
at Prime Hook (Delaware) and Cape May (New Jersey) National Wildlife 
Refuges, key Delaware Bay stopover areas, suggests that estuarine 
beaches would survive, but with increased vulnerability to storm surges 
as back marsh areas become inundated (Scarborough 2009, p. 61; Stern 
2009; pp. 7-9).
Mid-Atlantic--Delaware Bay Horseshoe Crab Habitat
    The narrow sandy beaches used by spawning horseshoe crabs in 
Delaware Bay are diminishing at sometimes rapid rates due to beach 
erosion as a product of land subsidence and sea level rise (CCSP 2009b, 
p. 207). At Maurice Cove, New Jersey, for example, portions of the 
shoreline eroded at a rate of 14.1 ft (4.3 m) per year from 1842 to 
1992. Another estimate for this area suggests the shoreline retreated 
about 500 ft (150 m) landward in a 32-year period, exposing ancient 
peat deposits that are considered suboptimal spawning habitat for the 
horseshoe crab. Particularly if human infrastructure along the coast 
leaves estuarine beaches little room to migrate inland as sea level 
rises, further loss of spawning habitat is likely (CCSP 2009b, p. 207).
    At present, the degree to which horseshoe crab populations will 
decline as beaches are lost remains unclear. Botton et al. (1988, p. 
331) found that even subtle alteration of the sediment, such as through 
erosion, may affect the suitability of habitat for horseshoe crab 
reproduction, and that horseshoe crab spawning activity is lower in 
areas where erosion has exposed underlying peat (Botton et al. 1988, p. 
325). Through habitat modeling, Czaja (2009, p. 9) found overall 
horseshoe crab habitat suitability in Delaware Bay was lower with a 
3.9-ft (1.2-m) sea level rise than a 2-ft (0.6-m) rise, although this 
study did not attempt to account for landward migration. Research 
suggests that horseshoe crabs can successfully reproduce in alternate 
habitats (other than estuarine beaches), such as sandbars and the sandy 
banks of tidal creeks (CCSP 2009b, p. 82). However, these habitats may 
provide only a temporary refuge for horseshoe crabs if the alternate 
habitats eventually become inundated as well (CCSP 2009b, p. 82). In 
addition, these alternate spawning habitats may not be conducive to 
foraging red knots, or may not be available in sufficient amounts to 
support red knot and other shorebird populations during spring 
    In 2012, Delaware Bay lost considerable horseshoe crab spawning 
habitat during Hurricane Sandy. A team of biologists found a 70 percent 
decrease in optimal horseshoe crab spawning habitat (Niles et al. 2012, 
p. 1). Several areas were eroded to exposed sod bank or rubble (used in 
shoreline stabilization), which do not provide suitable spawning 
habitat. Creek mouths may now constitute the bulk of the remaining 
intact spawning areas (Dey pers. comm., December 3, 2012). However, any 
conclusions about the long-term effects of this storm are premature due 
to the highly dynamic nature of the shoreline.
United States--Southeast and the Gulf Coast
    Rates of erosion for the Southeast Atlantic region are generally 
highest in South Carolina along barrier islands and headland shores 
associated with the Santee delta. Erosion is also rapid along some 
barrier islands in North Carolina. The highest rates of erosion in 
Florida are generally localized around tidal inlets (Morton and Miller 
2005, p. 1). Looking at 17 recreational beaches in North Carolina and 3 
local sea level rise scenarios, Bin (et al. 2007, p. 9) projected 10 to 
30 percent increases in beach erosion by 2030, and 20 to 60 percent 
increases by 2080. These authors assumed a constant coastwide rate of 
erosion, no barrier island migration, and no beach nourishment or 
hardening (Bin et al. 2007, p. 8).
    The barrier islands in the Georgia Bight (southern South Carolina 
to northern Florida) are generally higher in elevation, wider, and more 
geologically stable than the microtidal barriers found elsewhere along 
the Atlantic coast (Leatherman, 1989, p. 2-15). This lower 
vulnerability to sea level rise is generally reflected in the CVI 
(table 2). The most stable Southeast Atlantic beaches are along the 
east coast of Florida due to low wave energy, but also due to frequent 
beach nourishment (Morton and Miller 2005, p. 1), which can have both 
beneficial and adverse effects on red knot habitat as discussed in the 
section that follows. Although Florida's Atlantic coast in general is 
more stable than other portions of the red knot's U.S. range, localized 
changes from sea level rise can be significant. Modeling (SLAMM 6) of a 
3.3-ft (1-m) sea level rise by 2011 at Merritt Island National Wildlife 
Refuge (which supports red knots) projects a 47 percent loss of 
estuarine beach habitats (USFWS 2011d, p. 13).
    In contrast to the more stable southern Atlantic shores of Georgia 
and Florida, the Gulf coast is the lowest-lying area in the United 
States and consequently the most sensitive to small changes in sea 
level (Leatherman 1989, p. 2-15). Sediment compaction and oil and gas 
extraction in the Gulf have compounded tectonic subsidence, leading to 
greater rates of relative sea level rise (Hopkinson et al. 2008, p. 
255; Morton 2003, pp. 21-22; Morton et al. 2003, p. 77; Penland and 
Ramsey 1990, p. 323). In addition, areas with small tidal ranges are 
the most vulnerable to loss of intertidal wetlands and flats induced by 
sea level rise (USEPA 2013; Thieler and Hammar-Klose 2000; Thieler and 
Hammar-Klose 1999). Tidal range along the Gulf coast is very low, less 
than 3.3 ft (1 m) in some areas.
    In Alabama, coastal land loss is caused primarily by beach and 
bluff erosion, but other mechanisms for loss, such as submergence, 
appear to be minor. Barrier islands in Mississippi are migrating 
laterally and erosion rates are accelerating; island areas have been

[[Page 60035]]

reduced by about one-third since the 1850s (Morton et al. 2004, p. 29).
    Erosion is rapid along some barrier islands and headlands in Texas 
(Morton et al. 2004, p. 4). Texas loses approximately 5 to 10 ft (1.5 
to 3 m) of beach per year, as the high water line shifts landward 
(Higgins 2008, p. 49). Sea level rise was cited as a contributing 
factor in a 68 percent decline in tidal flats and algal mats in the 
Corpus Christi area (i.e., Lamar Peninsula to Encinal Peninsula) in 
Texas from the 1950s to 2004 (Tremblay et al. 2008, p. 59). Long-term 
erosion at an average rate of -5.9  4.3 ft (1.8  1.3 m) per year characterizes 64 percent of the Texas Gulf 
shoreline. Although only 48 percent of the shoreline experienced short-
term erosion, the average short-term erosion rate of -8.5 ft (-2.6 m) 
per year is higher than the long-term rate, indicating accelerated 
erosion in some areas. Erosion of Gulf beaches in Texas is concentrated 
between Sabine Pass and High Island, downdrift (southwest) of the 
Galveston Island seawall, near Sargent Beach and Matagorda Peninsula, 
and along South Padre Island. The most stable or accreting beaches in 
Texas are on southwestern Bolivar Peninsula, Matagorda Island, San Jose 
Island, and central Padre Island (Morton et al. 2004, p. 32).
    Rates of erosion for the U.S. Gulf coast are generally highest in 
Louisiana along barrier island and headland shores associated with the 
Mississippi delta (Morton et al. 2004, p. 4). Louisiana has the most 
rapid rate of beach erosion in the country (Leatherman 1989, p. 2-15). 
Subsidence and coastal erosion are functions of both natural and human-
induced processes. About 90 percent of the Louisiana Gulf shoreline is 
experiencing erosion, which increased from an average of -26.9  14.4 ft (-8.2  4.4 m) per year in the long term to 
an average of -39.4 ft (-12.0 m) per year in the short term. Short 
sections of the shoreline are accreting as a result of lateral island 
migration, while the highest rates of erosion in Louisiana coincide 
with subsiding marshes and migrating barrier islands such as the 
Chandeleur Islands, Caminada-Moreau headland, and the Isles Dernieres 
(Morton et al. 2004, p. 31).
    Compared to shoreline erosion in some other Gulf coast states, the 
average long-term erosion rate of -2.5  3.0 ft (-0.8  0.9 m) per year for west Florida is low, primarily because wave 
energy is low. Although erosion rates are generally low, more than 50 
percent of the shoreline is experiencing both long-term and short-term 
erosion. The highest erosion rates on Florida's Gulf coast are 
typically localized near tidal inlets, a preferred red knot habitat 
(see the ``Migration and Wintering Habitat'' section of the Rufa Red 
Knot Ecology and Abundance supplemental document). Long-term and short-
term trends and rates of shoreline change are similar where there has 
been little or no alteration of the sediment supply or littoral system 
(e.g., Dog Island, St. George Island, and St. Joseph Peninsula). 
Conversely, trends and rates of change have shifted from long-term 
erosion to short-term stability or accretion where beach nourishment is 
common (e.g., Longboat Key, Anna Maria Island, Sand Key, and 
Clearwater, Panama City Beach, and Perdido Key). Slow but chronic 
erosion along the west coast of Florida eventually results in narrowing 
of the beaches (Morton et al. 2004, pp. 27, 29).
    Strauss et al. (2012, p. 4) found more than 78 percent of the 
coastal dry land and freshwater wetlands on land less than 3.3 ft (1 m) 
above local Mean High Water in the continental United States is located 
in Louisiana, Florida, North Carolina, and South Carolina.
United States--Summary
    Important red knot habitats tend to occur along higher-
vulnerability portions of the U.S. shoreline. Red knot habitats along 
the Atlantic coast of New Jersey, Virginia, and the Carolinas and along 
the Gulf coast west of Florida are at particular risk from sea level 
rise. Delaware Bay is projected to lose substantial shorebird habitat 
by mid-century, even under moderate scenarios of sea level rise. In 
many areas, red knot coastal habitats are expected to migrate inland 
under a mid-range estimate (3.3-ft; 1-m) of sea level rise, except 
where constrained by topography, coastal development, or shoreline 
stabilization structures. Some areas may see short- or long-term net 
increases in red knot habitat, but low-lying and narrow islands become 
more prone to disintegration as sea level rise accelerates, which may 
produce local or regional net losses of habitat. The upper range (6.6 
ft; 2 m) of current predictions was not evaluated, but would be 
expected to exceed the migration capacity of many more red knot 
habitats than the 3.3-ft (1-m) scenario.
Sea Level Rise--Summary
    Due to background rates of sea level rise and the naturally dynamic 
nature of coastal habitats, we conclude that red knots are adapted to 
moderate (although sometimes abrupt) rates of habitat change in their 
wintering and migration areas. However, rates of sea level rise are 
accelerating beyond those that have occurred over recent millennia. In 
most of the red knot's nonbreeding range, shorelines are expected to 
undergo dramatic reconfigurations over the next century as a result of 
accelerating sea level rise. Extensive areas of marsh are likely to 
become inundated, which may reduce foraging and roosting habitats. 
Marshes may be able to establish farther inland, but the rate of new 
marsh formation (e.g., intertidal sediment accumulation, development of 
hydric soils, colonization of marsh vegetation) may be slower than the 
rate of deterioration of existing marsh, particularly under the higher 
sea level rise scenarios. The primary red knot foraging habitats, 
intertidal flats and sandy beaches, will likely be locally or 
regionally inundated, but replacement habitats are likely to reform 
along the shoreline in its new position. However, if shorelines 
experience a decades-long period of high instability and landward 
migration, the formation rate of new beach habitats may be slower than 
the inundation rate of existing habitats. In addition, low-lying and 
narrow islands (e.g., in the Caribbean and along the Gulf and Atlantic 
coasts) may disintegrate rather than migrate, representing a net loss 
of red knot habitat. Superimposed on these changes are widespread human 
attempts to stabilize the shoreline, which are known to exacerbate 
losses of intertidal habitats by blocking their landward migration. The 
cumulative loss of habitat across the nonbreeding range could affect 
the ability of red knots to complete their annual cycles, possibly 
affecting fitness and survival, and is thereby likely to negatively 
influence the long-term survival of the rufa red knot.
Factor A--U.S. Shoreline Stabilization and Coastal Development
    Much of the U.S. coast within the range of the red knot is already 
extensively developed. Direct loss of shorebird habitats occurred over 
the past century as substantial commercial and residential developments 
were constructed in and adjacent to ocean and estuarine beaches along 
the Atlantic and Gulf coasts. In addition, red knot habitat was also 
lost indirectly, as sediment supplies were reduced and stabilization 
structures were constructed to protect developed areas.
    Sea level rise and human activities within coastal watersheds can 
lead to long-term reductions in sediment supply to the coast. The 
damming of rivers, bulk-heading of highlands, and armoring of coastal 
bluffs have reduced erosion in natural source areas and consequently 
the sediment loads reaching coastal areas. Although it is

[[Page 60036]]

difficult to quantify, the cumulative reduction in sediment supply from 
human activities may contribute substantially to the long-term 
shoreline erosion rate. Along coastlines subject to sediment deficits, 
the amount of sediment supplied to the coast is less than that lost to 
storms and coastal sinks (inlet channels, bays, and upland deposits), 
leading to long-term shoreline recession (Coastal Protection and 
Restoration Authority of Louisiana 2012, p. 18; Florida Oceans and 
Coastal Council 2010, p. 7; CCSP 2009b, pp. 48-49, 52-53; Defeo et al. 
2009, p. 6; Morton et al. 2004, pp. 24-25; Morton 2003, pp. 11-14; 
Herrington 2003, p. 38; Greene 2002, p. 3).
    In addition to reduced sediment supplies, other factors such as 
stabilized inlets, shoreline stabilization structures, and coastal 
development can exacerbate long-term erosion (Herrington 2003, p. 38). 
Coastal development and shoreline stabilization can be mutually 
reinforcing. Coastal development often encourages shoreline 
stabilization because stabilization projects cost less than the value 
of the buildings and infrastructure. Conversely, shoreline 
stabilization sometimes encourages coastal development by making a 
previously high-risk area seem safer for development (CCSP 2009b, p. 
87). Protection of developed areas is the driving force behind ongoing 
shoreline stabilization efforts. Large-scale shoreline stabilization 
projects became common in the past 100 years with the increasing 
availability of heavy machinery. Shoreline stabilization methods change 
in response to changing new technologies, coastal conditions, and 
preferences of residents, planners, and engineers. Along the Atlantic 
and Gulf coasts, an early preference for shore-perpendicular structures 
(e.g., groins) was followed by a period of construction of shore-
parallel structures (e.g., seawalls), and then a period of beach 
nourishment, which is now favored (Morton et al. 2004, p. 4; Nordstrom 
2000, pp. 13-14).
    Past and ongoing stabilization projects fundamentally alter the 
naturally dynamic coastal processes that create and maintain beach 
strand and bayside habitats, including those habitat components that 
red knots rely upon. Past loss of stopover and wintering habitat likely 
reduce the resilience of the red knot by making it more dependent on 
those habitats that remain, and more vulnerable to threats (e.g., 
disturbance, predation, reduced quality or abundance of prey, increased 
intraspecific and interspecific competition) within those restricted 
habitats. (See Factors C and E, below, for discussions of these 
threats, many of which are intensified in and near developed areas.)
Shoreline Stabilization--Hard Structures
    Hard structures constructed of stone, concrete, wood, steel, or 
geotextiles have been used for centuries as a coastal defense strategy 
(Defeo et al. 2009, p. 6). The most common hard stabilization 
structures fall into two groups: structures that run parallel to the 
shoreline (e.g., seawalls, revetments, bulkheads) and structures that 
run perpendicular to the shoreline (e.g., groins, jetties). Groins are 
often clustered in groin fields, and are intended to protect a finite 
section of beach, while jetties are normally constructed at inlets to 
keep sand out of navigation channels and provide calm-water access to 
harbor facilities (U.S. Army Corps of Engineers (USACE) 2002, pp. I-3-
13, 21). Descriptions of the different types of stabilization 
structures can be found in Rice (2009, pp. 10-13), Herrington (2003, 
pp. 66-89), and USACE (2002, Parts V and VI).
    Prior to the 1950s, the general practice in the United States was 
to use hard structures to protect developments from beach erosion or 
storm damages (USACE 2002, p. I-3-21). The pace of constructing new 
hard stabilization structures has since slowed considerably (USACE 
2002, p. V-3-9). Many states within the range of the red knot now 
discourage or restrict the construction of new, hard oceanfront 
protection structures, although the hardening of bayside shorelines is 
generally still allowed (Kana 2011, p. 31; Greene 2002, p. 4; Titus 
2000, pp. 742-743). Most existing hard oceanfront structures continue 
to be maintained, and some new structures continue to be built. Eleven 
new groin projects were approved in Florida from 2000 to 2009 (USFWS 
2009, p. 36). Since 2006 a new terminal groin has been constructed at 
one South Carolina site, three groins have been approved but not yet 
constructed in conjunction with a beach nourishment project, and a 
proposed new terminal groin is under review (M. Bimbi pers. comm. 
January 31, 2013). The State of North Carolina prohibited the use of 
hard erosion control structures in 1985, but 2011 legislation 
authorized an exception for construction of up to four new terminal 
groins (Rice 2012a, p. 7). While some states have restricted new 
construction, hard structures are still among the alternatives in the 
Federal shore protection program (USACE 2002, pp. V-3-3, 7).
    Hard shoreline stabilization projects are typically designed to 
protect property (and its human inhabitants), not beaches (Kana 2011, 
p. 31; Pilkey and Howard 1981, p. 2). Hard structures affect beaches in 
several ways. For example, when a hard structure is put in place, 
erosion of the oceanfront sand continues, but the fixed back-beach line 
remains, resulting in a loss of beach area (USACE 2002, p. I-3-21). In 
addition, hard structures reduce the regional supply of beach sediment 
by restricting natural sand movement, further increasing erosion 
problems (Morton et al. 2004, p. 25; Morton 2003, pp. 19-20; Greene 
2002, p. 3). Through effects on waves and currents, sediment transport 
rates, Aeolian (wind) processes, and sand exchanges with dunes and 
offshore bars, hard structures change the erosion-accretion dynamics of 
beaches and constrain the natural migration of shorelines (CCSP 2009b, 
pp. 73, 81-82; 99-100; Defeo et al. 2009, p. 6; Morton 2003, pp. 19-20; 
Scavia et al. 2002, p. 152; Nordstrom 2000, pp. 98-107, 115-118). There 
is ample evidence of accelerated erosion rates, pronounced breaks in 
shoreline orientation, and truncation of the beach profile downdrift of 
perpendicular structures--and of reduced beach widths (relative to 
unprotected segments) where parallel structures have been in place over 
long periods of time (Hafner 2012, pp. 11-14; CCSP 2009b, pp. 99-100; 
Morton 2003, pp. 20-21; Scavia et al. 2002, p. 159; USACE 2002, pp. V-
3-3, 7; Nordstrom 2000, pp. 98-107; Pilkey and Wright 1988, pp. 41, 57-
59). In addition, marinas and port facilities built out from the shore 
can have effects similar to hard stabilization structures (Nordstrom 
2000, pp. 118-119).
    Structural development along the shoreline and manipulation of 
natural inlets upset the naturally dynamic coastal processes and result 
in loss or degradation of beach habitat (Melvin et al. 1991, pp. 24-
25). As beaches narrow, the reduced habitat can directly lower the 
diversity and abundance of biota (life forms), especially in the upper 
intertidal zone. Shorebirds may be impacted both by reduced habitat 
area for roosting and foraging, and by declining intertidal prey 
resources, as has been documented in California (Defeo et al. 2009, p. 
6; Dugan and Hubbard 2006, p. 10). In an estuary in England, Stillman 
et al. (2005, pp. 203-204) found that a two to eight percent reduction 
in intertidal area (the magnitude expected through sea level rise and 
industrial developments including extensive stabilization structures) 
decreased the predicted

[[Page 60037]]

survival rates of five out of nine shorebird species evaluated 
(although not of Calidris canutus).
    In Delaware Bay, hard structures also cause or accelerate loss of 
horseshoe crab spawning habitat (CCSP 2009b, p. 82; Botton et al. in 
Shuster et al. 2003, p. 16; Botton et al. 1988, entire), and shorebird 
habitat has been, and may continue to be, lost where bulkheads have 
been built (Clark in Farrell and Martin 1997, p. 24). In addition to 
directly eliminating red knot habitat, hard structures interfere with 
the creation of new shorebird habitats by interrupting the natural 
processes of overwash and inlet formation. Where hard stabilization is 
installed, the eventual loss of the beach and its associated habitats 
is virtually assured (Rice 2009, p. 3), absent beach nourishment, which 
may also impact red knots as discussed below. Where they are 
maintained, hard structures are likely to significantly increase the 
amount of red knot habitat lost as sea levels continue to rise.
    In a few isolated locations, however, hard structures may enhance 
red knot habitat, or may provide artificial habitat. In Delaware Bay, 
for example, Botton et al. (1994, p. 614) found that, in the same 
manner as natural shoreline discontinuities like creek mouths, jetties 
and other artificial obstructions can act to concentrate drifting 
horseshoe crab eggs and thereby attract shorebirds. Another example 
comes from the Delaware side of the bay, where a seawall and jetty at 
Mispillion Harbor protect the confluence of the Mispillion River and 
Cedar Creek. These structures create a low energy environment in the 
harbor, which seems to provide highly suitable conditions for horseshoe 
crab spawning over a wider variation of weather and sea conditions than 
anywhere else in the bay (G. Breese pers. comm. March 25, 2013). 
Horseshoe crab egg densities at Mispillion Harbor are consistently an 
order of magnitude higher than at other bay beaches (Dey et al. 2011a, 
p. 8), and this site consistently supports upwards of 15 to 20 percent 
of all the knots recorded in Delaware Bay (Lathrop 2005, p. 4). In 
Florida, A. Schwarzer (pers. comm. March 25, 2013) has observed 
multiple instances of red knots using artificial structures such as 
docks, piers, jetties, causeways, and construction barriers; we have no 
information regarding the frequency, regularity, timing, or 
significance of this use of artificial habitats. Notwithstanding 
localized red knot use of artificial structures, and the isolated case 
of hard structures improving foraging habitat at Mispillion Harbor, the 
nearly universal effect of such structures is the degradation or loss 
of red knot habitat.
Shoreline Stabilization--Mechanical Sediment Transport
    Several types of sediment transport are employed to stabilize 
shorelines, protect development, maintain navigation channels, and 
provide for recreation (Gebert 2012, pp. 14, 16; Kana 2011, pp. 31-33; 
USACE 2002, p. I-3-7). The effects of these projects are typically 
expected to be relatively short in duration, usually less than 10 
years, but often these actions are carried out every few years in the 
same area, resulting in a more lasting impact on habitat suitability 
for shorebirds. Mechanical sediment transport practices include beach 
nourishment, sediment backpassing, sand scraping, and dredging, and 
each practice is discussed below.
Sediment Transport--Beach Nourishment
    Beach nourishment is an engineering practice of deliberately adding 
sand (or gravel or cobbles) to an eroding beach, or the construction of 
a beach where only a small beach, or no beach, previously existed (NRC 
1995, pp. 23-24). Since the 1970s, 90 percent of the Federal 
appropriation for shore protection has been for beach nourishment 
(USACE 2002, p. I-3-21), which has become the preferred course of 
action to address shoreline erosion in the United States (Kana 2011, p. 
33; Morton and Miller 2005, p. 1; Greene 2002, p. 5). Beach nourishment 
requires an abundant source of sand that is compatible with the native 
beach material. The sand is trucked to the target beach, or 
hydraulically pumped using dredges (Hafner 2012, p. 21). Sand for beach 
nourishment operations can be obtained from dry land-based sources; 
estuaries, lagoons, or inlets on the backside of the beach; sandy 
shoals in inlets and navigation channels; nearshore ocean waters; or 
offshore ocean waters; with the last two being the most common sources 
(Greene 2002, p. 6).
    Where shorebird habitat has been severely reduced or eliminated by 
hard stabilization structures, beach nourishment may be the only means 
available to replace any habitat for as long as the hard structures are 
maintained (Nordstrom and Mauriello 2001, entire), although such 
habitat will persist only with regular nourishment episodes (typically 
on the order of every 2 to 6 years). In Delaware Bay, beach nourishment 
has been recommended to prevent loss of spawning habitat for horseshoe 
crabs (Kalasz 2008, p. 34; Carter et al. in Guilfoyle et al. 2007, p. 
71; Atlantic States Marine Fisheries Commission (ASMFC) 1998, p. 28), 
and is being pursued as a means of restoring shorebird habitat in 
Delaware Bay following Hurricane Sandy (Niles et al. 2013, entire; 
USACE 2012, entire). Beach nourishment was part of a 2009 project to 
maintain important shorebird foraging habitat at Mispillion Harbor, 
Delaware (Kalasz pers. comm. March 29, 2013; Siok and Wilson 2011, 
entire). However, red knots may be directly disturbed if beach 
nourishment takes place while the birds are present. On New Jersey's 
Atlantic coast, beach nourishment has typically been scheduled for the 
fall, when red knots are present, because of various constraints at 
other times of year. In addition to causing disturbance during 
construction, beach nourishment often increases recreational use of the 
widened beaches that, without careful management, can increase 
disturbance of red knots. Beach nourishment can also temporarily 
depress, and sometimes permanently alter, the invertebrate prey base on 
which shorebirds depend. These effects (disturbance, reduced food 
resources) are discussed further under Factor E, below.
    In addition to disturbing the birds and impacting the prey base, 
beach nourishment can affect the quality and quantity of red knot 
habitat (M. Bimbi pers. comm. November 1, 2012; Greene 2002, p. 5). The 
artificial beach created by nourishment may provide only suboptimal 
habitat for red knots, as a steeper beach profile is created when sand 
is stacked on the beach during the nourishment process. In some cases, 
nourishment is accompanied by the planting of dense beach grasses, 
which can directly degrade habitat, as red knots require sparse 
vegetation to avoid predation. By precluding overwash and Aeolian 
transport, especially where large artificial dunes are constructed, 
beach nourishment can also lead to further erosion on the bayside and 
promote bayside vegetation growth, both of which can degrade the red 
knot's preferred foraging and roosting habitats (sparsely vegetated 
flats in or adjacent to intertidal areas). Preclusion of overwash also 
impedes the formation of new red knot habitats. Beach nourishment can 
also encourage further development, bringing further habitat impacts, 
reducing future alternative management options such as a retreat from 
the coast, and perpetuating the developed and stabilized conditions 
that may ultimately lead to inundation where beaches are prevented from

[[Page 60038]]

migrating (M. Bimbi pers. comm. November 1, 2012; Greene 2002, p. 5).
    Following placement of sediments much coarser than those native to 
the beach, Peterson et al. (2006, p. 219) found that the area of 
intertidal-shallow subtidal shorebird foraging habitat was reduced by 
14 to 29 percent at a site in North Carolina. Presence of coarse shell 
material armored the substrate surface against shorebird probing, 
further reducing foraging habitat by 33 percent, and probably also 
inhibiting manipulation of prey when encountered by a bird's bill 
(Peterson et al. 2006, p. 219). (In addition to this physical change 
from adding coarse sediment, nourishment that places sediment 
dissimilar to the native beach also substantially increases impacts to 
the red knot's invertebrate prey base; see Factor E--Reduced Food 
Availability--Sediment Placement.) Lott (2009, p. viii) found a strong 
negative correlation between sand placement projects and the presence 
of piping plovers (Charadrius melodus) (nonbreeding) and snowy plovers 
(Charadrius alexandrinus) (breeding and nonbreeding) in Florida.
Sediment Transport--Backpassing and Scraping
    Sediment backpassing is a technique that reverses the natural 
migration of sediment by mechanically (via trucks) or hydraulically 
(via pipes) transporting sand from accreting, downdrift areas of the 
beach to eroding, updrift areas of the beach (Kana 2011, p. 31; Chasten 
and Rosati 2010, p. 5). Currently less prevalent than beach 
nourishment, sediment backpassing is an emerging practice because 
traditional nourishment methods are beginning to face constraints on 
budgets and sediment availability (Hafner 2012, pp. 31, 35; Chase 2006, 
p. 19). Beach bulldozing or scraping is the process of mechanically 
redistributing beach sand from the littoral zone (along the edge of the 
sea) to the upper beach to increase the size of the primary dune or to 
provide a source of sediment for beaches that have no existing dune; no 
new sediment is added to the system (Kana 2011, p. 30; Greene 2002, p. 
5; Lindquist and Manning 2001, p. 4). Beach scraping tends to be a 
localized practice. In Florida beach scraping is usually used only in 
emergencies such as after hurricanes and other storms, but in New 
Jersey this practice is more routine in some areas.
    Many of the effects of sediment backpassing and beach scraping are 
similar to those for beach nourishment (USFWS 2011c, pp. 11-24; 
Lindquist and Manning 2001, p. 1), including disturbance during and 
after construction, alteration of prey resources, reduced habitat area 
and quality, and precluded formation of new habitats. Relative to beach 
nourishment, sediment backpassing and beach scraping can involve 
considerably more driving of heavy trucks and other equipment on the 
beach including areas outside the sand placement footprint, potentially 
impacting shorebird prey resources over a larger area (see Factor E, 
below, for discussion of vehicle impacts on prey resources) (USFWS 
2011c, pp. 11-24). In addition, these practices can directly remove 
sand from red knot habitats, as is the case in one red knot 
concentration area in New Jersey (USFWS 2011c, p. 27). Backpassing and 
sand scraping can involve routine episodes of sand removal or transport 
that maintain the beach in a narrower condition, indefinitely reducing 
the quantity of back-beach roosting habitat.
Sediment Transport--Dredging
    Sediments are also manipulated to maintain navigation channels. 
Many inlets in the U.S. range of the red knot are routinely dredged and 
sometimes relocated. In addition, nearshore areas are routinely dredged 
(``mined'') to obtain sand for beach nourishment. Regardless of the 
purpose, inlet and nearshore dredging can affect red knot habitats. 
Dredging often involves removal of sediment from sand bars, shoals, and 
inlets in the nearshore zone, directly impacting optimal red knot 
roosting and foraging habitats (Harrington 2008, p. 2; Harrington in 
Guilfoyle et al. 2007, pp. 18-19; Winn and Harrington in Guilfoyle et 
al. 2006, pp. 8-11). These ephemeral habitats are even more valuable to 
red knots because they tend to receive less recreational use than the 
main beach strand (see Factor E--Human Disturbance, below).
    In addition to causing this direct habitat loss, the dredging of 
sand bars and shoals can preclude the creation and maintenance of red 
knot habitats by removing sand sources that would otherwise act as 
natural breakwaters and weld onto the shore over time (Hayes and Michel 
2008, p. 85; Morton 2003, p. 6). Further, removing these sand features 
can cause or worsen localized erosion by altering depth contours and 
changing wave refraction (Hayes and Michel 2008, p. 85), potentially 
degrading other nearby red knot habitats indirectly because inlet 
dynamics exert a strong influence on the adjacent shorelines. Studying 
barrier islands in Virginia and North Carolina, Fenster and Dolan 
(1996, p. 294) found that inlet influences extend 3.4 to 8.1 mi (5.4 to 
13.0 km), and that inlets dominate shoreline changes for up to 2.7 mi 
(4.3 km). Changing the location of dominant channels at inlets can 
create profound alterations to the adjacent shoreline (Nordstrom 2000, 
p. 57).
Shoreline Stabilization and Coastal Development--Existing Extent
Existing Extent--Atlantic Coast
    The mid-Atlantic coast from New York to Virginia is the most 
urbanized shoreline in the country, except for parts of Florida and 
southern California. In New York and New Jersey, hard structures and 
beach nourishment programs cover much of the coastline. Farther south, 
there are more undeveloped and preserved sections of coast (Leatherman 
1989, p. 2-15). Along the entire Atlantic, most of the ocean coast is 
fully or partly (intermediate) developed, less than 10 percent is in 
conservation, and about one-third is undeveloped and still available 
for new development (see table 3).
    By area, more than 80 percent of the land below 3.3 ft (1 m) in 
Florida and north of Delaware is developed or intermediate. In 
contrast, only 45 percent of the land from Georgia to Delaware is 
developed or intermediate (Titus et al. 2009, p. 3). However, the 55 
percent undeveloped coast in this southern region includes sparsely 
developed portions of the Chesapeake Bay, and the bay sides of 
Albermarle and Pamlico Sounds in North Carolina (Titus et al. 2009, p. 
4), which do not typically support large numbers of red knots 
(eBird.org 2012). Instead, red knots tend to concentrate along the 
ocean coasts (eBird.org 2012), which are more heavily developed (Titus 
et al. 2009, p. 4) even in the Southeast. Conservation lands account 
for most of the Virginia ocean coast, and large parts of Massachusetts, 
North Carolina, and Georgia, including several key red knot stopover 
and wintering areas. The proportion of undeveloped land is generally 
greater at the lowest elevations, except along New Jersey's Atlantic 
coast (Titus et al. 2009, p. 3).
    New Jersey's Atlantic coast has the longest history of stabilized 
barrier island shoreline in North America. It also has the most 
developed coastal barriers and the highest degree of stabilization in 
the United States (Nordstrom 2000, p. 3). As measured by the amount of 
shoreline in the 90 to 100 percent stabilized category, New Jersey is 
43 percent hard-stabilized (Pilkey and Wright 1988, p. 46). Of New 
Jersey's 130 mi (209 km) of coast, 98 mi (158 km) (75 percent) are 
developed (including 48 mi (77 km) with ongoing beach

[[Page 60039]]

nourishment programs), 25 mi (40 km) are preserved (including several 
areas with existing hard structures), and 7 mi (11 km) are inlets 
(Gebert 2012, p. 32). Nearly 27 mi (43.5 km) are protected by shore-
parallel structures (Nordstrom 2000, pp. 21-22), including 5.6 mi (9 
km) of revetments and seawalls, and there are 24 inlet jetties, 368 
groins, and 1 breakwater (Hafner 2012, p. 42).
    Although much less developed than New Jersey's Atlantic coast, 
Delaware Bay does have many areas of bulkheads, groins, and jetties 
(Botton et al. in Shuster et al. 2003, p. 16). Beach stabilization 
structures such as bulkheads and riprap account for 4 percent of the 
Delaware shoreline and 5.6 percent of the New Jersey side. An 
additional 2.9 and 3.4 percent of the Delaware and New Jersey 
shorelines, respectively, also have some form of armoring in the back-
beach. About 8 percent of the Delaware bayshore is subject to near-
shore development. While some beaches in New Jersey and Delaware have 
had development removed, new development and redevelopment continues on 
the Delaware side of the bay (Niles et al. 2008, p. 40). New Jersey has 
not conducted beach nourishment in the Delaware Bay, but Delaware has a 
standing nourishment program in the Bay, and its beaches have been 
regularly nourished since 1962. Approximately 3 million cubic yards 
(yd\3\; 2.3 million cubic meters (m\3\)) of sand have been placed on 
Delaware Bay beaches in Delaware over the past 40 years (Smith et al. 
2002a, p. 5). In 2010, the State of Delaware completed a 10-year 
management plan for Delaware Bay beaches, with ongoing nourishment 
recommended as the key measure to protect coastal development (Delaware 
Department of Natural Resources and Environmental Control 2010, p. 4).

  Table 3--Percent * of Dry Land Within 3.3 ft (1 m) of High Water by Intensity of Development Along the United
                                              States Atlantic Coast
                                            [Titus et al. 2009, p. 5]
                                                     Developed     Intermediate     Undeveloped    Conservation
Massachusetts...................................              26              29              22              23
Rhode Island....................................              36              11              48               5
Connecticut.....................................              80               8               7               5
New York........................................              73              18               4               6
New Jersey......................................              66              15              12               7
Pennsylvania....................................              49              21              26               4
Delaware........................................              27              26              23              24
Maryland........................................              19              16              56               9
District of Columbia............................              82               5              14               0
Virginia........................................              39              22              32               7
North Carolina..................................              28              14              55               3
South Carolina..................................              28              21              41              10
Georgia.........................................              27              16              23              34
Florida.........................................              65              10              12              13
Coastwide.......................................              42              15              33               9
* Percentages may not add up to 100 due to rounding.

Existing Extent--Southeast Atlantic and Gulf Coasts
    The U.S. southeastern coast from North Carolina to Florida is the 
least urbanized along the Atlantic coast, although both coasts of 
Florida are urbanizing rapidly. Texas has the most extensive sandy 
coastline in the Gulf, and much of the area is sparsely developed 
(Leatherman 1989, p. 2-15). Table 4 gives the miles of developed and 
undeveloped beach from North Carolina to Texas. (Note the difference 
between tables 3 and 4; table 3 gives all dry land within 3.3 ft (1 m) 
of high water, while table 4 is limited to sandy, oceanfront beaches.) 
Regionwide, about 40 percent of the southeast and Gulf coast is already 
developed, as shown in table 4. Not all of the remaining 60 percent in 
the ``undeveloped'' category, however, is still available for 
development because about 43 percent (about 910 miles) of beaches 
across this region are considered preserved. Preserved beaches include 
those in public or nongovernmental conservation ownership and those 
under conservation easements.
    The 43 percent of preserved beaches generally overlap with the 
undeveloped beach category (1,264 miles or 60 percent, as shown in 
table 4), but may also include some developed areas such as 
recreational facilities or private inholdings within parks (USFWS 
2012a, p. 15). To account for such recreational or inholding 
development, we rounded down the estimated preserved, undeveloped 
beaches to about 40 percent. Adding the preserved, undeveloped 40 
percent estimate to the 40 percent that is already developed, we 
conclude that only about 20 percent of the beaches from North Carolina 
to Texas are still undeveloped and available for new development. 
Looking at differences in preservation rates across this region, 
Georgia and the Mississippi barrier islands have the highest 
percentages of preserved beaches (76 and 100 percent of shoreline 
miles, respectively), Alabama and the Mississippi mainland have the 
lowest percentages (24 and 25 percent of shoreline miles, 
respectively), and all other States have between 30 and 55 percent of 
their beach mileage in some form of preservation (USFWS 2012a, p. 15). 
Table 5 shows the extent of southeast and Gulf coast shoreline with 
shore-parallel structures, beach nourishment, or both.

[[Page 60040]]

  Table 4--The Lengths and Percentages of Sandy, Oceanfront Beach That Are Developed and Undeveloped Along the
                                       Southeast Atlantic and Gulf Coasts
                   [T. Rice pers. comm. January 3, 2013; Rice 2012a, p. 6; USFWS 2012a, p. 15]
                                         Miles of         Miles and  percent of         Miles and  percent of
                State                    shoreline           developed beach             undeveloped beach *
North Carolina......................             326  159 (49%)...................  167 (51%)
South Carolina......................             182  93 (51%)....................  89 (49%)
Georgia.............................              90  15 (17%)....................  75 (83%)
Florida.............................             809  459 (57%)...................  351 (43%)
Alabama.............................              46  25 (55%)....................  21 (45%)
Mississippi barrier island..........              27  0 (0%)......................  27 (100%)
Mississippi mainland **.............              51  41 (80%)....................  10 (20%)
Louisiana...........................             218  13 (6%).....................  205 (94%)
Texas...............................             370  51 (14%)....................  319 (86%)
Coastwide...........................           2,119  856 (40%)...................  1,264 (60%)
* Beaches classified as ``undeveloped'' occasionally include a few scattered structures.
** The mainland Mississippi coast along Mississippi Sound includes 51.3 mi of sandy beach as of 2010-2011, out
  of approximately 80.7 total shoreline miles (the remaining portion is nonsandy, either marsh or armored
  coastline with no sand).

  Table 5--Approximate Shoreline Miles of Sandy, Oceanfront Beach That Have Been Modified by Armoring With Hard
   Erosion Control Structures, and by Sand Placement Activities, North Carolina to Texas, as of December 2011
                                     [Rice 2012a, p. 7; USFWS 2012a, p. 24]
                                                Known  approximate  miles of      Known  approximate  miles of
                                             armored beach  (percent  of total   beach receiving sand placement
                                                         coastline)              (percent  of total  coastline)
North Carolina.............................  Not available....................  91.3 (28%)
South Carolina.............................  Not available....................  67.6 (37%)
Georgia....................................  10.5 (12%).......................  5.5 (6%)
Florida....................................  117.3 *..........................  379.6 (47%)
Alabama....................................  4.7(10%).........................  7.5 (16%)
Mississippi barrier island.................  0 (0%)...........................  1.1 (4%)
Mississippi mainland.......................  45.4 (89%).......................  43.5 (85%)
Louisiana..................................  15.9 (7%)........................  60.4 (28%)
Texas......................................  36.6 (10%).......................  28.3 (8%)
    Total *................................  230.4 *..........................  684.8 (32%)
* Partial data.

Existing Extent--Inlets
    Of the nation's top 50 ports active in foreign waterborne commerce, 
over 90 percent require regular dredging. Over 392 million yd\3\ (300 
million m\3\) of dredged material are removed from navigation channels 
each year, not including inland waterways. Most inlets and harbors used 
for commercial navigation in the United States are protected and 
stabilized by hard structures (USACE 2002, p. I-3-7). In New Jersey, 
many inlets that existed around 1885 and all inlets that formed since 
that time were artificially closed or kept from reopening after natural 
closure (Nordstrom 2000, p. 19). Five of the 12 New Jersey inlets that 
now exist are stabilized by jetties, and 2 of the unstabilized jetties 
are maintained by dredging (Nordstrom 2000, p. 20). Table 6 gives the 
condition of inlets from North Carolina to Texas.

                                  Table 6--Inlet Condition Along the Southeast Atlantic and Gulf Coasts, December 2011
                                                                   [Rice 2012b, p. 8]
                                                                                      Existing inlets
                                                                                              Habitat modification type                     Artificially
                                                 Number of    Number of  ------------------------------------------------------------------    closed
                                                   inlets      modified    Structures                                         Artificially
                                                                inlets         *         Dredged     Relocated      Mined        opened
North Carolina................................           20     17 (85%)            7           16            3            4             2            11
South Carolina................................           47     21 (45%)           17           11            2            3             0             1
Georgia.......................................           23      6 (26%)            5            3            0            1             0             0
Florida east..................................           21     19 (90%)           19           16            0            3            10             0
Florida west..................................           48     24 (50%)           20           22            0            6             7             1

[[Page 60041]]

Alabama.......................................            4     4 (100%)            4            3            0            0             0             2
Mississippi...................................            6      5 (67%)            0            4            0            0             0             0
Louisiana.....................................           34     10 (29%)            7            9            1            2             0            46
Texas.........................................           18     14 (78%)           10           13            2            1            11             3
    Total.....................................          221    119 (54%)     89 (40%)     97 (44%)       8 (4%)      20 (9%)      30 (14%)            64
* Structures include jetties, terminal groins, groin fields, rock or sandbag revetments, seawalls, and offshore breakwaters.

Shoreline Stabilization and Coastal Development--Future Practices
    As shown in tables 3 and 4 and explained above, much of the 
Atlantic and Gulf coasts are approaching ``buildout,'' the condition 
that exists when all available land is either developed or preserved 
and no further development is possible. Table 3 shows that about one-
third of dry land within 3.3 ft (1 m) of high tide on the Atlantic 
coast is still available for development (i.e., not already developed 
or preserved), but the percent of developable land in or near red knot 
habitats is probably lower because oceanfront beach areas are already 
more developed than other lands in this dataset (see Titus et al. 2009, 
p. 4). Focused on beach habitats, USFWS (2012a, p. 15) found that only 
about 20 percent of the coast from North Carolina to Texas is available 
for development. In light of sea level rise, it is unclear the extent 
to which these remaining lands will be developed over the next few 
decades. Several states already regulate or restrict new coastal 
development (Titus et al. 2009, p. 22; Higgins 2008, pp. 50-53).
    However, development pressures continue, driven by tourism 
(Nordstrom 2000, p. 3; New Jersey Department of Environmental 
Protection (NJDEP) 2010, p. 1; Gebert 2012, pp. 14, 16), as well as 
high coastal population densities and rapid population growth. For 
example, 35 million people--1 of 8 people in the United States--live 
within 100 mi (161 km) of the New Jersey shore (Gebert 2012, p. 17). Of 
the 25 most densely populated U.S. counties, 23 are along a coast 
(USEPA 2012). Population density along the coast is more than five 
times greater than in inland areas, and coastal populations are 
expected to grow another 9 percent by 2020 (NOAA 2012b). Coastal 
population density was greatest in the Northeast as of 2003, but 
population growth from 1980 to 2003 was greatest in the Southeast 
(Crossett et al. 2004, pp. 4-5).
    Although the likely extent of future coastal development is highly 
uncertain, continued efforts to protect existing and any new 
developments is more certain, at least over the next 10 to 20 years. As 
shown in tables 3 and 4, about 40 percent of the coast within the U.S. 
range of the red knot is already developed, and much of this area is 
protected by hard or soft means, or both. Shoreline stabilization over 
the near term is likely to come primarily through the maintenance of 
existing hard structures along with beach nourishment programs. As 
described below, it is unknown if these practices can be sustained in 
the longer term (CCSP 2009b, p. 87), but protection efforts seem likely 
to continue over shorter timeframes (Kana 2011, p. 34; Titus et al. 
2009, pp. 2-3; Leatherman 1989, p. 2-27).
    States have shown a commitment to beach nourishment that is likely 
to persist. Of the 18 Atlantic and Gulf coast States with federally 
approved Coastal Zone Management Programs, 16 have beach nourishment 
policies. Nine of these 18 States have a continuing funding program for 
beach nourishment, and 6 more fund projects on a case-by-case basis 
(Higgins 2008, p. 55). Annual State appropriations for beach 
nourishment are $25 million in New Jersey and $30 million in Florida 
(Gebert 2012, p. 18). Beach nourishment has become the default solution 
to beach erosion because oceanfront property values have risen many 
times faster than the cost of nourishment (Kana 2011, p. 34). The cost 
of sand delivery has risen about tenfold since 1950, while oceanfront 
property values rose about 1,000-fold over the same timeframe. As long 
as these trends persist, beach nourishment will remain more cost 
effective than property abandonment (Kana 2011, p. 34; Titus et al. 
1991, p. 26). Over the next 50 years, Wakefield and Parsons (2002, pp. 
5, 8) project that a retreat from the coast (i.e., relocation, 
abandonment of buildings and infrastructure, or both) in Delaware would 
cost three times more than a continued beach nourishment program, 
assuming no decline in cost due to technological advance and no 
increase due to diminished availability of borrow sediment or 
accelerated sea level rise.
    In attempting to infer the likely future quantity of red knot 
habitat, major sources of uncertainty are when and where the practice 
of routine beach nourishment may become unsustainable and how 
communities will respond. It is uncertain whether beach nourishment 
will be continued into the future due to economic constraints, as well 
as often limited supplies of suitable sand resources (CCSP 2009b, p. 
49). Despite the current commitment to beach nourishment, it does seem 
likely that this practice will eventually become unsustainable. Given 
rising sea levels and increased intensity of storms predicted by 
climate change models, a steady increase in beach replenishment would 
be needed to maintain usable beaches and protect coastal development 
(NJDEP 2010, p. 3). For example, New Jersey has seen a steady increase 
in costs and volumes of sand since the 1970s (NJDEP 2010, p. 2). For 
the case where the rate of sea level rise continues to increase, as has 
been projected by several recent studies, perpetual nourishment becomes 
impossible since the time between successive nourishment episodes 
continues to decrease (Weggel 1986, p. 418).
    Even if it remains physically possible for beach nourishment to 
keep pace with sea level rise, this option may be constrained by cost 
and sand availability (Pietrafesa 2012, entire; NJDEP 2010, p. 2; Titus 
et al. 1991, entire; Leatherman 1989, entire). For example, there is a 
large deficit of readily available, nearshore sand in some coastal 
Florida counties (Florida Oceans and Coastal Council 2010, p. 15). To 
maintain Florida beaches in coming years, local governments will 
increasingly be forced to look for

[[Page 60042]]

suitable sand in other regions of the State and from more expensive or 
nontraditional sources, such as deeper waters, inland sand mines, or 
the Bahamas. In Florida's Broward and Miami-Dade Counties, there is 
estimated to be a net deficit of 34 million yd\3\ (26 million m\3\) of 
sand over the next 50 years (Florida Oceans and Coastal Council 2010, 
p. 15).
    For the Atlantic and Gulf coasts, Titus et al. (1991, p. 24) 
estimated the cumulative cost of beach nourishment in 2100 at $14 
billion to $69 billion for a 1.6-ft (0.5-m) sea level rise; $25 billion 
to $119 billion for a 3.3-ft (1-m) rise; and $56 to $230 billion for a 
6.6-ft (2-m) rise. At similar rates of sea level rise, projected costs 
reach at least $4.1 billion to $10.2 billion by 2040, not adjusted for 
inflation (Leatherman 1989, p. 2-24). As these cumulative cost 
projections were produced around 1990, we divided by 110 for Titus et 
al. (1991, p. 24) and by 50 for Leatherman (1989, p. 2-24) to infer a 
range of estimated annual costs of $82 million to $2.1 billion in 1990 
dollars, or about $135 million to $3.5 billion in 2009 dollars (U.S. 
Bureau of Labor Statistics 2009). For comparison, Congressional 
appropriations for beach nourishment projects and studies around 2009 
totaled about $150 million per fiscal year (NOAA 2009), with the 
Federal share typically covering 65 percent of a beach nourishment 
project (NOAA 2000, p. 9), for a total public expenditure of about $231 
million. Thus, public spending around 2009 was above the minimum that 
is expected to be necessary to keep pace with 0.5-m sea level rise 
($135 million), but was far below the maximum estimated cost to 
maintain beaches under the 2-m rise scenario ($3.5 billion). In recent 
years, Federal funding has not kept pace with some states' demands for 
beach nourishment (NJDEP 2010, p. 3).
    Table 7 shows the estimated nationwide quantities of sand needed to 
maintain current beaches (including the Pacific and Hawaii, which 
constitute a small part of the total) through nourishment under various 
sea level rise scenarios. Tremendous quantities of good quality sand 
would be necessary to maintain the nation's beaches. These estimates 
are especially remarkable given that only about 562 million yd\3\ (430 
million m\3\) of sand were placed from 1922 to 2003 (Peterson and 
Bishop 2005, p. 887). Almost all of this sand must be derived from 
offshore, but as of 1989 only enough sand had been identified to 
accommodate the two lowest sea level rise scenarios over the long term. 
In addition, available offshore sand is not distributed evenly along 
the U.S. coast, so some areas will run out of local (the least 
expensive) sand in a few decades. Costs of beach nourishment increase 
substantially if sand must be acquired from considerable distance from 
the beach requiring nourishment (Leatherman 1989, p. 2-21). Further, 
much more sand would be required to stabilize the shore if barrier 
island disintegration or segmentation occur (CCSP 2009b, p. 102).

   Table 7--Cumulative Nationwide Estimates of Sand Quantities Needed (in Millions of Cubic Yards) To Maintain
                   Current Beaches Through Nourishment Under Various Sea Level Rise Scenarios
                                           [Leatherman 1989; p. 2-24]
                                                   2.01 ft (0.6    3.65 ft (1.1    5.30 ft (1.6    6.94 ft (2.1
       Global sea level rise by 2100/year               m)              m)              m)              m)
2020............................................             405             531             654             778
2040............................................             750           1,068           1,395           1,850
2100............................................           2,424           4,345           6,768           9,071

    Under current policies, protection of coastal development is 
standard practice. However, coastal communities were designed and built 
without recognition of rising sea levels. Most protection structures 
are designed for current sea level and may not accommodate a 
significant rise (CCSP 2009b, p. 100). Policymakers have not decided 
whether the practice of protecting development should continue as sea 
level rises, or be modified to avoid adverse environmental consequences 
and increased costs of protecting coastal development (CCSP 2009b, p. 
87; Titus et al. 2009, entire). It is unclear at what point different 
areas may be forced by economics or sediment availability to move 
beyond beach nourishment (Leatherman 1989, p. 2-27). Due to lower costs 
and sand recycling, sediment backpassing may prolong the ability of 
communities to maintain artificial beaches in some areas. However, in 
those times and places that artificial beach maintenance is abandoned, 
the remaining alternatives would likely be limited to either a retreat 
from the coast or increased use of hard structures to protect 
development (CCSP 2009b, p. 87; Defeo et al. 2009, p. 7; Wakefield and 
Parsons 2002, p. 2). Retreat is more likely in areas of lower-density 
development, while in areas of higher-density development, the use of 
hard structures may expand substantially (Florida Oceans and Coastal 
Council 2010, p. 16; Titus et al. 2009, pp. 2-3; Defeo et al. 2009, p. 
7; Wakefield and Parsons 2002, p. 2). The quantity of red knot habitat 
would be markedly decreased by a proliferation of hard structures. Red 
knot habitat would be significantly increased by retreat, but only 
where hard stabilization structures do not exist or where they get 
    Hurricane Sandy recovery efforts show that retreat is not yet being 
contemplated as an option on the highly developed coasts of New York 
and New Jersey (Martin 2012, entire; Regional Plan Association, p. 1), 
and underscore the looming sand shortage that may preclude the 
continuation of beach nourishment as it has been practiced over recent 
decades (Dean 2012, entire).
Shoreline Stabilization and Coastal Development--Summary
    About 40 percent of the U.S. coastline within the range of the red 
knot is already developed, and much of this developed area is 
stabilized by a combination of existing hard structures and ongoing 
beach nourishment programs. In those portions of the range for which 
data are available (New Jersey and North Carolina to Texas), about 40 
percent of inlets, a preferred red knot habitat, are hard-stabilized, 
dredged, or both. Hard stabilization structures and dredging degrade 
and often eliminate existing red knot habitats, and in many cases 
prevent the formation of new shorebird habitats. Beach nourishment may 
temporarily maintain suboptimal shorebird habitats where they would 
otherwise be lost as a result of hard structures, but beach nourishment 
also has adverse effects to red knots and their habitats. Demographic 
and economic pressures remain strong to continue existing programs of 
shoreline stabilization, and to develop additional areas, with an 
estimated 20 to 33

[[Page 60043]]

percent of the coast still available for development. However, we 
expect existing beach nourishment programs will likely face eventual 
constraints of budget and sediment availability as sea level rises. In 
those times and places that artificial beach maintenance is abandoned, 
the remaining alternatives would likely be limited to either a retreat 
from the coast or increased use of hard structures to protect 
development. The quantity of red knot habitat would be markedly 
decreased by a proliferation of hard structures. Red knot habitat would 
be significantly increased by retreat, but only where hard 
stabilization structures do not exist or where they get dismantled. The 
cumulative loss of habitat across the nonbreeding range could affect 
the ability of red knots to complete their annual cycles, possibly 
affecting fitness and survival, and is thereby likely to negatively 
influence the long-term survival of the rufa red knot.
Factor A--International Coastal Development
    The red knot's breeding area is very sparsely developed, and 
development is not considered a threat in this part of the subspecies' 
range. We have little information about coastal development in the red 
knot's non-U.S. migration and wintering areas, compared to U.S. 
migration and wintering areas. However, escalating pressures caused by 
the combined effects of population growth, demographic shifts, economic 
development, and global climate change pose unprecedented threats to 
sandy beach ecosystems worldwide (DeFeo et al. 2009, p. 1; Schlacher et 
al. 2008a, p. 70).
International Development--Canada
    Cottage-building to support tourism and expansion of suburbs is 
taking place along coastal areas of the Bay of Fundy (Provinces of New 
Brunswick and Nova Scotia) (WHSRN 2012), an important staging area for 
red knots (Niles et al. 2008, p. 30). In addition, the Bay of Fundy 
supports North America's only tidal electric generating facility that 
uses the ``head'' created between the water levels at high and low tide 
to generate electricity (National Energy Board 2006, p. 38). The 20-
megawat (MW) Annapolis Tidal Power Plant in Nova Scotia Province is a 
tidal barrage design, involving a large dam across the river mouth 
(Nova Scotia Power 2013). Tidal energy helps reduce emissions of 
greenhouse gases. However, tidal barrage projects can be intrusive to 
the area surrounding the catch basins (the area into which water flows 
as the tide comes in), resulting in erosion and silt accumulation 
(National Energy Board 2006, pp. 39-40).
    Although there is good potential for further tidal barrage 
development in Nova Scotia, with at least two more prospects in the 
northeast part of the Bay of Fundy, environmental and land use impacts 
would be carefully assessed. There are no current plans to develop 
these areas, but Nova Scotia and New Brunswick Provinces and some 
northeastern U.S. States are studying potential for power generation 
from tidal currents in the Maritime region (National Energy Board 2006, 
p. 40). Today, engineers are moving away from tidal barrage designs, in 
favor of new technologies like turbines that are anchored to the ocean 
floor. From 2009 to 2010, the Minas Passage in the Bay of Fundy 
supported a 1-MW in-stream tidal turbine. There is considerable 
interest in exploring the full potential of this resource (Nova Scotia 
Energy 2013). The potential impacts to red knot habitat from in-stream 
generation designs are likely less than barrage designs. However, 
without careful siting and design, potential for habitat loss exists 
from the terrestrial development that would likely accompany such 
    At another important red knot stopover, James Bay, barging has been 
proposed in connection with diamond mining developments near 
Attawapiskat on the west coast of the bay. Barging could affect river 
mouth habitats (COSEWIC 2007, p. 37), for example, through wake-induced 
International Development--Central and South America
    Moving from north to south, below is the limited information we 
have about development in the red knot's Central and South American 
migration and wintering areas.
    In the Costa del Este area of Panama City, Panama, an important 
shorebird area, prime roosting sites were lost to housing development 
in the mid-2000s (Niles et al. 2008, p. 73). Development is occurring 
at a rapid rate around Panama Bay, and protections for the bay were 
recently reduced (Cosier 2012).
    Due to the region's remoteness, relatively little is known about 
threats to red knot habitat in Maranh[atilde]o, Brazil. Among the key 
threats that can be identified to date are offshore petroleum 
exploration on the continental shelf (also see Factor E--Oil Spills and 
Leaks, and Environmental Contaminants, below), as well as iron ore and 
gold mining. These activities lead to loss and degradation of coastal 
habitat through the dumping of soil and urban spread along the coast. 
Mangrove clearing has also had a negative impact on red knot habitat by 
altering the deposition of sediments, which leads to a reduction in 
benthic (bottom-dwelling) prey (WHSRN 2012; Niles et al. 2008, p. 97; 
COSEWIC 2007, p. 37). Threats to shorebird habitat also exist from salt 
extraction operations (WHSRN 2012). In addition to industrial 
development, some areas with good access have potential for tourism; 
however, most areas are inaccessible (WHSRN 2012).
    Development is a threat to red knot stopover habitat along the 
Patagonian coast of Argentina. In the Bah[iacute]a Samboromb[oacute]n 
reserve, Argentina's northernmost red knot stopover site, threats come 
from urban and agrosystem expansion and development (Niles et al. 2008, 
p. 98).
    Further south, the beaches along Bah[iacute]a San Antonio, 
Argentina, are a key red knot stopover (Niles et al. 2008, p. 19). The 
City of San Antonio Oeste has nearly 20,000 inhabitants and many more 
seasonal visitors (WHSRN 2012). Just one beach on Bah[iacute]a San 
Antonio draws 300,000 tourists every summer, a number that has 
increased 20 percent per year over the past decade. New access points, 
buildings, and tourist amusement facilities are being constructed along 
the beach. Until recently, there was little planning for this rapid 
expansion. In 2005, the first urban management plan for the area 
advised restricted use of land close to key shorebird areas, which 
include extensive dune parks. Public land ownership includes the City's 
shoreline, beaches, and a regional port for shipping produce and soda 
ash (WHSRN 2012).
    Habitat loss and deterioration are among the threats confronting 
the urban shorebird reserves at R[iacute]o Gallegos, an important red 
knot site in Patagonia (Niles et al. 2008, p. 19). As the city of 
R[iacute]o Gallegos grew toward the coast, ecologically productive 
tidal flats and marshes were filled for housing and used as urban solid 
waste dumps and disposal sites for untreated sewage, leading to the 
loss of roosting areas and the loss and modification of the feeding 
areas (WHSRN 2012; Niles et al. 2008, p. 98; Ferrari et al. 2002, p. 
39), in part as a result of wind-blown trash from a nearby landfill 
being deposited in shorebird habitats (Niles et al. 2008, p. 98; 
Ferrari et al. 2002, p. 39) (see Factor E--Environmental Contaminants). 
While the creation of the reserve stopped most of these development 
practices, the lots that had been approved prior to the reserve's 
establishment have continued to be filled. In addition, a public works 
project to treat the previously dumped

[[Page 60044]]

effluents is under construction, necessitating the use of heavy 
equipment and the crossing of several stretches of salt marshes and mud 
flats used by the shorebirds. Activities outside the shorebird reserve 
also have potential to impact red knots. While the tidal flat and salt 
marsh zones most important to shorebirds are located within the 
reserves, the land uses of adjacent areas include recreation, fishing, 
cattle ranching, urban development, and three ports. In an effort to 
address some of these concerns, local institutions and various 
nongovernmental organizations are working together to reassess the 
coastal environment and promote its management and conservation (WHSRN 
    Two of Argentina's Patagonian provinces (R[iacute]o Negro that 
includes San Antonio Oeste, and Santa Cruz that includes R[iacute]o 
Gallegos) have declared the conservation of migratory shorebirds to be 
``in the Provincial interest'' and made it illegal to modify wetland 
habitat important for shorebirds (WHSRN 2011).
    Ongoing development continues to encroach in parts of Argentinean 
Tierra del Fuego, an important red knot wintering area (Niles et al. 
2008, p. 17). In the area called Pasos de las Cholgas, the land 
immediately behind the coast has been divided, and two homes are under 
construction. Over time, if no urban management plan is developed, 
development of this area could affect red knots and their habitat. 
South of Pasos de las Cholgas to the mouth of the Carmen Silva River 
(Chico), shorebirds have disappeared and trash is deposited by the wind 
from the city landfill. The municipality of R[iacute]o Grande is 
working on relocating the landfill. Also nearby, a methanol and urea 
plant are under construction, with plans to build two seaports, one for 
the company and another for the public. Between Cape Domingo and Cape 
Pe[ntilde]as is the City of R[iacute]o Grande, population 80,000. In 
the past 25 years, the city has increased its industrial economic 
growth and, in turn, its population. This rapid growth was not guided 
by an urban management plan. The coast shows signs of deterioration 
from industrial activities and effects from port construction, 
quarries, a concrete plant, trash dumps, plants and pipelines for 
wastewater treatment, and debris. R[iacute]o Grande City is working 
closely with the Provincial government to reverse the coastal 
degradation. One of the projects under way is the construction of an 
interpretive trail along the coast that teaches visitors about the 
marine environment and wetlands, and the importance of migratory birds 
as indicators of healthy environments (WHSRN 2012).
International Development--Summary
    Relative to the United States, little is known about development-
related threats to the red knot's nonbreeding habitat in other 
countries. Residential and recreational development is occurring along 
the Bay of Fundy in Canada, a red knot stopover site. The Bay of Fundy 
also has considerable potential for the expansion of electric 
generation from tidal energy, but new power plant developments are 
likely to minimize environmental impacts relative to older designs. 
Industrial development is considered a threat to red knot habitat along 
the north coast of Brazil, but relatively little is known about this 
region. Urban development is a localized threat to red knot habitats in 
Panama, along the Patagonian coast of Argentina, and in the Argentinean 
portion of Tierra del Fuego. Over the past decade, shorebird 
conservation efforts, including the establishment of shorebird reserves 
and the initiation of urban planning, have begun in many of these 
areas. However, human population and development continue to grow in 
many areas. In some key wintering and stopover sites, development 
pressures are likely to exacerbate the habitat impacts caused by sea 
level rise (discussed previously).
Factor A--Beach Cleaning
    On beaches that are heavily used for tourism, mechanical beach 
cleaning (also called beach grooming or raking) is a common practice to 
remove wrack (seaweed and other organic debris are deposited by the 
tides), litter, and other natural or manmade debris by raking or 
sieving the sand, often with heavy equipment (Defeo et al. 2009, p. 4). 
Beach raking became common practice in New Jersey in the late 1980s 
(Nordstrom and Mauriello 2001, p. 23) and is increasingly common in the 
Southeast, especially in Florida (M. Bimbi pers. comm. November 1, 
2012). Wrack removal and beach raking both occur on the Gulf beach side 
of the developed portion of South Padre Island in the Lower Laguna 
Madre in Texas (USFWS 2012a, p. 28), a well-documented red knot habitat 
(Newstead et al. in press). On the Southeast Atlantic and Gulf coasts, 
beach cleaning occurs on private beaches and on some municipal or 
county beaches that are used by red knots (M. Bimbi pers. comm. 
November 1, 2012). Most wrack removal on state and Federal lands is 
limited to post-storm cleanup and does not occur regularly (USFWS 
2012a, p. 28).
    Practiced routinely, beach cleaning can cause considerable physical 
changes to the beach ecosystem. In addition to removing humanmade 
debris, beach cleaning and raking machines remove accumulated wrack, 
topographic depressions, emergent foredunes and hummocks, and sparse 
vegetation (USFWS 2012a, p. 28; Defeo et al. 2009, p. 4; Nordstrom and 
Mauriello 2001, p. 23; Nordstrom 2000, p. 53), all of which can be 
important microhabitats for shorebirds and their prey. Many of these 
changes promote erosion. Grooming loosens the beach surface by breaking 
up surface crusts (salt and algae) and lag elements (shells or gravel), 
and roughens or ``fluffs'' the sand, all of which increase the erosive 
effects of wind (Cathcart and Melby 2009, p. 14; Defeo et al. 2009, p. 
4; Nordstrom 2000, p. 53). Grooming can also result in abnormally broad 
unvegetated zones that are inhospitable to dune formation or plant 
colonization, thereby enhancing the likelihood of erosion (Defeo et al. 
2009, p. 4). By removing vegetation and wrack, cleaning machines also 
reduce or eliminate natural sand-trapping features, further 
destabilizing the beach (USFWS 2012a, p. 28; Nordstrom et al. 2006b, p. 
1266; Nordstrom 2000, p. 53). Further, the sand adhering to seaweed and 
trapped in the cracks and crevices of wrack is lost to the beach when 
the wrack is removed; although the amount of sand lost during a single 
sweeping activity is small, over a period of years this loss could be 
significant (USFWS 2012a, p. 28). Cathcart and Melby (2009, pp. i, 14) 
found that beach raking and grooming practices on mainland Mississippi 
beaches exacerbate the erosion process and shorten the time interval 
between beach nourishment projects (see discussion of shoreline 
stabilization, above). In addition to promoting erosion, raking also 
interferes with the natural cycles of dune growth and destruction on 
the beach (Nordstrom and Mauriello 2001, p. 23).
    Wrack removal also has significant ecological consequences, 
especially in regions with high levels of marine macrophyte (e.g., 
seaweed) production. The community structure of sandy beach 
macroinvertebrates can be closely linked to wrack deposits, which 
provide both a food source and a microhabitat refuge against 
desiccation (drying out). Wrack-associated animals, such as amphipods, 
isopods, and insects, are significantly reduced in species richness, 
abundance, and biomass by beach grooming (Defeo et al. 2009, p. 4). 
Invertebrates in the wrack are a primary prey base for some shorebirds 
such as

[[Page 60045]]

piping plovers (USFWS 2012a, p. 28), but generally make up only a 
secondary part of the red knot diet (see the ``Wintering and Migration 
Food'' section of the Rufa Red Knot Ecology and Abundance supplemental 
document). Overall shorebird numbers are positively correlated with 
wrack cover and the biomass of their invertebrate prey that feed on 
wrack; therefore, grooming can lower bird numbers (USFWS 2012a, p. 28; 
Defeo et al. 2009, p. 4). Due to their specialization on benthic, 
intertidal mollusks, red knots may be less impacted by these effects 
than some other shorebird species. However, removal of wrack may cause 
more significant localized effects to red knots at those times and 
places where abundant mussel spat are attached to deposits of tide-cast 
material, or where red knots become more reliant on wrack-associated 
prey species such as amphipods, insects, and marine worms. In Delaware 
Bay, red knots preferentially feed in the wrack line because horseshoe 
crab eggs become concentrated there (Nordstrom et al. 2006a, p. 438; 
Karpanty et al. 2011, pp. 990, 992); however, removal of wrack material 
is not practiced along Delaware Bay beaches (K. Clark pers. comm. 
February 11, 2013; A. Dey and K. Kalasz pers. comm. February 8, 2013). 
(More substantial threats to the red knot's prey resources are 
discussed under Factor E, below.)
    The heavy equipment used in beach grooming can cause disturbance to 
red knots (see Factor E--Human Disturbance, below). Only minimal 
disturbance is likely to occur on mid-Atlantic and northern Atlantic 
beaches because raking in these areas is most prevalent from Memorial 
Day to Labor Day, when only small numbers of red knots typically occur 
in this region.
    In summary, the practice of intensive beach raking may cause 
physical changes to beaches that degrade their suitability as red knot 
habitat. Removal of wrack may also have an effect on the availability 
of red knot food resources, particularly in those times and places that 
birds are more reliant on wrack-associated prey items. Beach cleaning 
machines are likely to cause disturbance to roosting and foraging red 
knots, particularly in the U.S. wintering range. Mechanized beach 
cleaning is widespread within the red knot's U.S. range, particularly 
in developed areas. We anticipate beach grooming may expand in some 
areas that become more developed but may decrease in other areas due to 
increasing environmental regulations, such as restrictions on beach 
raking in piping plover nesting areas (e.g., Nordstrom and Mauriello 
2001, p. 23).
Factor A--Invasive Vegetation
    Defeo et al. (2009, p. 6) cited biological invasions of both plants 
and animals as global threats to sandy beaches, with the potential to 
alter food webs, nutrient cycling, and invertebrate assemblages. 
Although the extent of the threat is uncertain, this may be due to poor 
survey coverage more than an absence of invasions. The propensity of 
invasive species to spread, and their tenacity once established, make 
them a persistent problem that is only partially countered by 
increasing awareness and willingness of beach managers to undertake 
control efforts (USFWS 2012a, p. 27). Like most invasive species, 
exotic coastal plants tend to reproduce and spread quickly and exhibit 
dense growth habits, often outcompeting native plants. If left 
uncontrolled, invasive plants can cause a habitat shift from open or 
sparsely vegetated sand to dense vegetation, resulting in the loss or 
degradation of red knot roosting habitat, which is especially important 
during high tides and migration periods. Many invasive species are 
either affecting or have the potential to affect coastal beaches (USFWS 
2012a, p. 27), and thus red knot habitat.
    Beach vitex (Vitex rotundifolia) is a woody vine introduced into 
the Southeast as a dune stabilization and ornamental plant that has 
spread from Virginia to Florida and west to Texas (Westbrooks and 
Madsen 2006, pp. 1-2). There are hundreds of beach vitex occurrences in 
North and South Carolina, and a small number of known locations in 
Georgia and Florida. Targeted beach vitex eradication efforts have been 
undertaken in the Carolinas (USFWS 2012a, p. 27). Crowfootgrass 
(Dactyloctenium aegyptium), which grows invasively along portions of 
the Florida coastline, forms thick bunches or mats that can change the 
vegetative structure of coastal plant communities and thus alter 
shorebird habitat (USFWS 2009, p. 37).
    Japanese (or Asiatic) sand sedge (Carex kobomugi) is a 4- to 12-in 
(10- to 30-cm) tall perennial sedge adapted to coastal beaches and 
dunes (Plant Conservation Alliance 2005, p. 1; Invasive Plant Atlas of 
New England undated). The species occurs from Massachusetts to North 
Carolina (U.S. Department of Agriculture (USDA) 2013) and spreads 
primarily by vegetative means through production of underground 
rhizomes (horizontal stems) (Plant Conservation Alliance 2005, p. 2). 
Japanese sand sedge forms dense stands on coastal dunes, outcompeting 
native vegetation and increasing vulnerability to erosion (Plant 
Conservation Alliance 2005, p. 1; Invasive Plant Atlas of New England 
undated). In the 2000s, Wootton (2009) documented rapid (exponential) 
growth in the spread of Japanese sand sedge at two New Jersey sites 
that are known to support shorebirds.
    Australian pine (Casuarina equisetifolia) is not a true pine, but 
is actually a flowering plant. Australian pine affects shorebirds by 
encroaching on foraging and roosting habitat and may also provide 
perches for avian predators (USFWS 2012a, p. 27; Bahamas National Trust 
2010, p. 1). Native to Australia and southern Asia, Australian pine is 
now found in all tropical and many subtropical areas of the world. This 
species occurs on nearly all islands of the Bahamas (Bahamas National 
Trust 2010, p. 2), and is among the three worst invasive exotic trees 
damaging wildlife habitat throughout South Florida (City of Sanibel 
undated). Growing well in sandy soils and salt tolerant, Australian 
pine is most common along shorelines (Bahamas National Trust 2010, p. 
2), where it grows in dense monocultures with thick mats of acidic 
needles (City of Sanibel undated). In the Bahamas, Australian pine 
often spreads to the edge of the intertidal zone, effectively usurping 
all shorebird roosting habitat (A. Hecht pers. comm. December 6, 2012). 
In addition to directly encroaching into shorebird habitats, Australian 
pine contributes to beach loss through physical alteration of the dune 
system (Stibolt 2011; Bahamas National Trust 2010, p. 2; City of 
Sanibel undated). The State of Florida prohibits the sale, transport, 
and planting of Australian pine (Stibolt 2011; City of Sanibel 
    In summary, red knots require open habitats that allow them to see 
potential predators and that are away from tall perches used by avian 
predators. Invasive species, particularly woody species, degrade or 
eliminate the suitability of red knot roosting and foraging habitats by 
forming dense stands of vegetation. Although not a primary cause of 
habitat loss, invasive species can be a regionally important 
contributor to the overall loss and degradation of the red knot's 
nonbreeding habitat.
Factor A--Agriculture and Aquaculture
    In some localized areas within the red knot's range, agricultural 
activities or aquaculture are impacting habitat quantity and quality. 
For example, on the Magdalen Islands, Canada (Province

[[Page 60046]]

of Quebec), clam farming is a new and growing local business. The clam 
farming location overlaps with the feeding grounds of transient red 
knots, and foraging habitats are being affected. Clam farming involves 
extracting all the juvenile clams from an area and relocating them in a 
``nursery area'' nearby. The top sand layer (upper 3.9 in (10 cm) of 
sand) is removed and filtered. Only the clams are kept, and the 
remaining fauna is rejected on the site. This disturbance of benthic 
fauna could affect foraging rates and weight gain in red knots by 
removing prey, disturbing birds, and altering habitat. This pilot clam 
farming project could expand into more demand for clam farming in other 
red knot feeding areas in Canada (USFWS 2011b, p. 23) (also see Factor 
E--Reduced Food Availability, below).
    Luckenbach (2007, p. 15) found that aquaculture of clams 
(Mercenaria mercenaria) in the lower Chesapeake Bay occurs in close 
proximity to shorebird foraging areas. The current distribution of clam 
aquaculture in the very low intertidal zone minimizes the amount of 
direct overlap with shorebird foraging habitats, but if clam 
aquaculture expands farther into the intertidal zone, more shorebird 
impacts (e.g., habitat alteration) may occur. However, these Chesapeake 
Bay intertidal zones are not considered the primary habitat for red 
knots (Cohen et al. 2009, p. 940), and red knots were not among the 
shorebirds observed in this study (Luckenbach 2007, p. 11). Likewise, 
oyster aquaculture is practiced in Delaware Bay (NJDEP 2011, pp. 1-10), 
but we have no information to indicate that this activity is affecting 
red knots.
    Shrimp (Family Penaeidae, mainly Litopenaeus vannamei) farming has 
expanded rapidly in Brazil in recent decades. Particularly since 1998, 
extensive areas of mangroves and salt flats, important shorebird 
habitats, have been converted to shrimp ponds (Carlos et al. 2010, p. 
1). In addition to causing habitat conversion, shrimp farm development 
has caused deforestation of river margins (e.g., for pumping stations), 
pollution of coastal waters, and changes in estuarine and tidal flat 
water dynamics (Campos 2007, p. 23; Zitello 2007, p. 21). Ninety-seven 
percent of Brazil's shrimp production is in the Northeast region of the 
country (Zitello 2007, p. 4). Carlos et al. (2010, p. 48) evaluated 
aerial imagery from 1988 to 2008 along 435 mi (700 km) of Brazil's 
northeast coastline in the States of Piau[iacute], Cear[aacute], and 
Rio Grande do Norte, covering 20 estuaries. Over this 20-year period, 
shrimp farms increased by 36,644 acres (ac) (14,829 hectares (ha)), 
while salt flats decreased by 34,842 ac (14,100 ha) and mangroves 
decreased by 2,876 ac (1,164 ha) (Carlos et al. 2010, pp. 54, 75).
    In the region of Brazil with the most intensive shrimp farming (the 
Northeast), newer surveys have documented more red knots than were 
previously known to use this area. In winter aerial surveys of 
Northeast Brazil in 1983, Morrison and Ross (1989, Vol. 2, pp. 149, 
183) documented only 15 red knots in the States of Cear[aacute], 
Piau[iacute], and eastern Maranh[atilde]o. However, ground surveys in 
the State of Cear[aacute] in December 2007 documented an average peak 
count of 481  31 red knots at just one site, Cajuais Bank 
(Carlos et al. 2010 pp. 10-11). Cajuais Bank also supports considerable 
numbers of red knots during migration, with an average peak count of 
434  95 in September 2007 (Carlos et al. 2010, pp. 10-11). 
Over this 1-year study, red knots were the most numerous shorebird at 
Cajuais Bank, accounting for nearly 25 percent of observations (Carlos 
et al. 2010, p. 9). Red knots that utilize Northeast Brazil were likely 
affected by recent habitat losses and degradation from the expansion of 
shrimp farming.
    Farther west along the North-Central coast of Brazil, the western 
part of Maranh[atilde]o and extending into the State of Par[aacute] is 
considered an important red knot concentration area during both winter 
and migration (D. Mizrahi pers. com. November 17, 2012; Niles et al. 
2008, p. 48; Baker et al. 2005, p. 12; Morrison and Ross 1989 Vol. 2, 
pp. 149, 183). Shrimp farm development has been far less extensive in 
Maranh[atilde]o and Par[aacute] than in Brazil's Northeast region 
(Campos 2007, pp. 3-4). However, rapid or unregulated expansion of 
shrimp farming in Maranh[atilde]o and Par[aacute] could pose an 
important threat to this key red knot wintering and stopover area 
(WHSRN 2012). In addition to aquaculture, some fishing is practiced in 
Maranh[atilde]o, but the area is fairly protected from conversion to 
land-based agriculture by its high salinity and inaccessibility (WHSRN 
2012). Fishing activities could potentially cause disturbance or alter 
habitat conditions.
    On the east coast of Brazil, Lagoa do Peixe serves as an important 
migration stopover for red knots. The abundance and availability of the 
red knot's food supply (snails) are dependent on the lagoon's water 
levels. The lagoon's natural fluctuations, and the coastal processes 
that allow for an annual connection of the lagoon with the sea, are 
altered by farmers draining water from farm fields into the lagoon. The 
hydrology of the lagoon is also affected by upland pine (Pinus spp.) 
plantations that cause siltation and lower the water table (Niles et 
al. 2008, pp. 97-98). These coastal habitats are also degraded by 
extensive upland cattle grazing, farming of food crops, and commercial 
shrimp farming. Fishermen also harvest from the lagoon and the sea, 
with trawlers setting nets along the coast (WHSRN 2012). Fishing 
activities could potentially cause disturbance or alter habitat 
    The red knot wintering and stopover area of R[iacute]o Gallegos is 
located on the south coast of Argentina. The lands surrounding the 
estuary have historically been used for raising cattle. During the past 
few years significant areas of brush land (that had served as a buffer) 
next to the shorebird reserve have been cleared and designated for 
agricultural use and the establishment of small farms. This loss of 
buffer areas may cause an increase in disturbance of the shorebirds 
(WHSRN 2012) because agricultural activities within visual distance of 
roosting or foraging shorebirds, including red knots, may cause the 
birds to flush.
    Grazing of the upland buffer is also a problem at Bah[iacute]a 
Lomas in Chilean Tierra del Fuego. The government owns all intertidal 
land and an upland buffer extending 262 ft (80 m) above the highest 
high tide, but ranchers graze sheep into the intertidal vegetation. 
Landowners have indicated willingness to relocate fencing to exclude 
sheep from the intertidal area and the upland buffer, but as of 2011, 
funding was needed to implement this work (L. Niles pers. comm. March 
2, 2011). Grazing in the intertidal zone could potentially displace 
roosting and foraging red knots, as well as degrade the quality of 
habitat through trampling, grazing, and feces.
    In summary, moderate numbers of red knots that winter or stopover 
in Northeast Brazil are likely impacted by past and ongoing habitat 
loss and degradation due to the rapid expansion of shrimp farming. 
Expansion of shrimp farming in North-Central Brazil, if it occurs, 
would affect far more red knots. Farming practices around Lagoa do 
Peixe are degrading habitats at this red knot stopover site, and 
localized clam farming in Canada could degrade habitat quality and prey 
availability for transient red knots. Agriculture is contributing to 
habitat loss and degradation at R[iacute]o Gallegos in Argentina, and 
probably at other localized areas within the range of the red knot. 
However, clam farming in the Chesapeake Bay does not appear to be 
impacting red knots at this time. Agriculture and aquaculture 
activities are a minor but locally important contributor to overall 
loss and

[[Page 60047]]

degradation of the red knot's nonbreeding habitat.
Factor A--Breeding Habitat Loss From Warming Arctic Conditions
    For several decades, surface air temperatures in the Arctic have 
warmed at approximately twice the global rate. Areas above 60 degrees 
([deg]) north latitude (around the middle of Hudson Bay) have 
experienced an average temperature increase of 1.8 to 3.6 degrees 
Fahrenheit ([deg]F) (1 to 2 degrees Celsius ([deg]C)) since a 
temperature minimum in the 1960s and 1970s (IPCC 2007c, p. 656). From 
1954 to 2003, mean annual temperatures across most of Arctic Canada 
increased by as much as 3.6 to 5.4 [deg]F (2 to 3 [deg]C), and warming 
in this region has been pronounced since 1966 (Arctic Climate Impact 
Assessment (ACIA) 2005, p. 1101). Increased atmospheric concentrations 
of greenhouse gases are ``very likely'' to have a larger effect on 
climate in the Arctic than anywhere else on the globe. (The ACIA (2005, 
pp. 607) report uses likelihood terminology similar, but not identical, 
to that used by the IPCC; see supplemental document--Climate Change 
Background--table 1). Under two mid-range emissions scenarios, models 
predict a mean global temperature increase of 4.5 to 6.3 [deg]F (2.5 to 
3.5 [deg]C) by 2100, while the predicted increase in the Arctic is 9 to 
12.6 [deg]F (5 to 7 [deg]C). Under both emission scenarios, arctic 
temperatures are predicted to rise 4.5 [deg]F (2.5 [deg]C) by mid-
century. Under the lower of these two emissions scenarios, some of the 
highest temperature increases in the Arctic (9 [deg]F; 5 [deg]C) in 
2100 are predicted to occur in the Canadian Archipelago (ACIA 2005, p. 
100), where the red knot breeds.
    To evaluate predicted changes in breeding habitat resulting from 
climate change, we note the eco-regional classification of the red 
knot's current breeding range. Most of the red knot's current breeding 
range (see supplemental document--Rufa Red Knot Ecology and Abundance--
figure 1, and Niles et al. 2008, p. 16) is classified as High Arctic, 
although some known and potential nesting areas are at the northern 
limits of the Low Arctic zone (CAFF 2010, p. 11). Based on mapping by 
the World Wildlife Fund (WWF) (2012) and modeling by Kaplan et al. 
(2003, p. 6), the red knot breeding range appears to correspond with 
the hemiarctic (i.e., ``middle Arctic'') zone described by ACIA (2005, 
p. 258). The region of known and potential breeding habitat is 
classified by the Canada Map Office (1989; 1993) as sparsely vegetated 
tundra, and most of the breeding range is classified by the WWF as 
Middle Arctic Tundra. Mapping by ACIA (2005, p. 5), based on Kaplan et 
al. (2003, entire), classifies almost all of the red knot breeding 
range as tundra, with only some small areas of potential breeding 
habitat on Melville and Bathurst Islands classified as polar desert. 
Kaplan et al. (2003, p. 6) mapped nearly all of the red knot breeding 
range as ``prostrate dwarf-shrub tundra,'' which is defined as 
discontinuous shrubland of prostrate (low-growing) deciduous shrubs, 0 
to 0.8 in (0 to 2 cm) tall, typically vegetated with willow (Salix 
spp.), avens (Dryas spp.), Pedicularis, Asteraceae, Caryophyllaceae, 
grasses, sedges, and true moss species (Kaplan et al. 2003, p. 3).
Arctic Warming--Eco-Regional Changes
    Arctic plants, animals, and microorganisms have adapted to climate 
change in the geologic past primarily by relocation, and their main 
response to future climate change is also likely to be through 
relocation. In many areas of the Arctic, however, relocation 
possibilities will likely be limited by regional and geographical 
barriers (ACIA 2005, p. 997). The Canadian High Arctic is characterized 
by land fragmentation within the archipelago and by large glaciated 
areas that can constrain species' movement and establishment (ACIA 
2005, p. 1012). Even if red knots are physically capable of relocating, 
some important elements of their breeding habitat (e.g., vegetative 
elements, prey species) may not have such capacity, and thus red knots 
may not be ecologically capable of relocation.
    Where their migration is not prevented by regional and geographic 
barriers, vegetation zones are generally expected to migrate north in 
response to warming conditions. Warming is ``very likely'' to lead to 
slow northward displacement of tundra by forests, while tundra will in 
turn displace High Arctic polar desert; tundra is projected to decrease 
to its smallest extent in the last 21,000 years, shrinking by a 
predicted 33 to 44 percent by 2100 (Feng et al. 2012, pp. 1359, 1366; 
Meltofte et al. 2007, p. 35; ACIA 2005, pp. 991, 998). Projections 
suggest that arctic ecosystems could change more in the next 100 years 
than they did over the last 6,000 years (Kaplan et al. 2003, pp. 1-2), 
which is longer than the rufa red knot is thought to have existed as a 
subspecies (Buehler et al. 2006, p. 485; Buehler and Baker 2005, p. 
505), suggesting that these ecosystem changes may exceed the knot's 
adaptive capacity.
    Arctic communities are ``very likely'' to respond strongly and 
rapidly to high-latitude temperature change (ACIA 2005, p. 257). The 
likely initial response of arctic communities to warming is an increase 
in the diversity of plants, animals, and microbes, but reduced 
dominance of currently widespread species (ACIA 2005, p. 263). Species 
that are important community dominants are likely to have a 
particularly rapid and strong effect on ecosystem processes where 
regional warming occurs. Hemiarctic plant species (those that occur 
throughout the Arctic, but most frequently in the middle Arctic) 
include several community dominants, such as grass, sedge, moss, and 
Dryas species (ACIA 2005, pp. 257-258), primary vegetative components 
of red knot nesting habitat (Niles et al. 2008, p. 27). Due to the 
current widespread distribution of these hemiarctic plants, their 
initial responses to climatic warming are likely to be increased 
productivity and abundance, probably followed by northward extension of 
their ranges (ACIA 2005, p. 257).
    Temperature is not the only factor that currently prevents some 
plant species from occurring in the Arctic. Latitude is also important, 
as life cycles depend not only on temperature but on the light regime 
as well. It is very likely that arctic species will tolerate warmer 
summers, whereas long day lengths will initially restrict the 
distribution of some subarctic species. This scenario will ``very 
likely'' cause new plant communities to arise with a novel species 
composition and structure, unlike any that exist now (ACIA 2005, p. 
    Studies have already documented shifts in arctic vegetation. For 
example, the ``greenness'' of North American tundra vegetation has 
increased during the period of satellite observations, 1982 to 2010 
(Walker et al. in Richter-Menge et al. 2011, p. 89). Over the 29-year 
record, North America saw an increase in the maximum Normalized 
Difference Vegetation Index (NDVI, a measure of vegetation 
photosynthetic capacity) but no significant shift in timing of peak 
greenness and no significant trend toward a longer growing season. 
However, whole-continent data can mask changes along latitudinal 
gradients and in different regions. For example, looking only at the 
Low Arctic (from 1982 to 2003), maximum NDVI showed about a 1-week 
shift in the initiation of ``green-up,'' and a somewhat higher NDVI 
late in the growing season. The Canadian High Arctic did not show 
earlier initiation of greenness, but did show a roughly 1- to

[[Page 60048]]

2-week shift toward earlier maximum NDVI (Walker et al. in Richter-
Menge et al. 2011, pp. 91-92). Several studies have also found 
increases in plant biomass linked to warming arctic temperatures 
(Epstein et al. 2012, p. 1; Hill and Henry 2011, p. 276; Hudson and 
Henry 2009, p. 2657). Observations from near the Lewis Glacier, Baffin 
Island, Canada, documented rapid vegetation changes along the margins 
of large retreating glaciers, and these changes may be partly 
responsible for large NDVI changes observed in northern Canada and 
Greenland (Bhatt et al. 2010, p. 2). Such ongoing changes to plant 
productivity will affect many aspects of arctic systems, including 
changes to active-layer depths, permafrost, and biodiversity (Bhatt et 
al. 2010, p. 2).
    In addition, the disappearance of dense ice cover on large parts of 
the Arctic Ocean may eliminate cooling effects on adjacent lands 
(Piersma and Lindstr[ouml]m 2004, p. 66) and may cause the High Arctic 
climate to become more maritime-dominated, a habitat condition in which 
few shorebirds breed (Meltofte et al. 2007, p. 36). Indeed, Bhatt et 
al. (2010, pp. 1-2) used NDVI to document temporal relationships 
between near-coastal sea ice, summer tundra land surface temperatures, 
and vegetation productivity. These authors found that changes in sea 
ice conditions have the strongest effect on ecosystems (e.g., 
accelerated warming, vegetation changes) immediately adjacent to the 
coast, but the terrestrial effects of sea ice changes also extend far 
inland. Ecosystems that are currently adjacent to year-round sea ice 
are likely to experience the greatest changes (Bhatt et al. 2010, pp. 
1-2). Summer sea-ice extent decreased by about 7 percent per decade 
from 1972 to 2002, the extent of multiyear sea ice has decreased, and 
ice thickness in the Arctic Basin has decreased by up to 40 percent 
since the 1950s and 1960s due to climate-related and other factors. 
Sea-ice extent is ``very likely'' to continue to decrease, with 
predictive modeling results ranging from loss of several percent to 
complete loss (ACIA 2005, p. 997). Based on data since 2001, Stroeve et 
al. (2012, p. 1005) suggested that the rate of sea ice loss is 
accelerating, and the National Aeronautics and Space Administration 
(NASA 2012) reported that the extent of summer sea ice in 2012 was the 
smallest on record (during the satellite era). As red knots typically 
nest near (within about 30 mi (50 km) of) arctic coasts (Niles et al. 
2008, p. 27; Niles et al. in Baker 2001, p. 14), their nesting habitats 
are vulnerable to accelerated temperature and vegetative changes and 
increasing maritime influence due to loss of sea ice.
    In addition to changes in plant communities and loss of sea ice, 
changes in freshwater hydrology of red knot breeding habitats are 
expected. Arctic freshwater systems, key foraging areas for red knots 
(Niles et al. 2008, p. 27), are particularly sensitive to even small 
changes in climatic regimes. Hydrologic processes may change gradually 
but may also respond abruptly as environmental thresholds are exceeded 
(ACIA 2005, p. 1012). Rising global temperatures are expected to result 
in permafrost degradation, possible decline in precipitation, and 
lowering of water tables, leading to drying of marshes and ponds in the 
southern parts of the Arctic (ACIA 2005, p. 418; Meltofte et al. 2007, 
p. 35). Conversely, thawing permafrost and increasing precipitation are 
very likely to increase the occurrence and distribution of shallow 
wetlands (ACIA 2005, p. 418) in other portions of the Arctic. We cannot 
predict the likely net changes in wetland availability within the red 
knot's breeding range over coming decades.
Arctic Warming--Effects on Red Knot Habitat
    In the long term, loss of tundra breeding habitat is a serious 
threat to shorebird species. The preferred habitats of shorebird 
populations that breed in the High Arctic are predicted to decrease or 
disappear as vegetation zones move northward (Meltofte et al. 2007, p. 
34; Lindstr[ouml]m and Agrell 1999, p. 145). High Arctic shorebirds 
such as the red knot seem to be particularly at risk, because the High 
Arctic already constitutes a relatively limited area ``squeezed in'' 
between the extensive Low Arctic biome and the Arctic Ocean (Meltofte 
et al. 2007, p. 35). In a circumpolar assessment of climate change 
impacts on Arctic-breeding waterbirds, Z[ouml]ckler and Lysenko (2000, 
pp. 5, 13) concluded that most of the Calidrid shorebirds (Calidris and 
related species) will not be able to adapt to shrubby or treelike 
habitats, but they note that habitat area may not be the most important 
factor limiting population size or breeding success.
    Potential impacts to shorebirds from changing arctic ecosystems go 
well beyond the loss of tundra breeding habitat (e.g., see Fraser et 
al. 2013; entire; Schmidt et al. 2012, p. 4421; Meltofte et al. 2007, 
p. 35; Ims and Fuglei 2005, entire). In the southern Arctic, loss of 
freshwater habitats may have more immediate effects on shorebird 
populations than the expansion of shrubs and trees (Meltofte et al. 
2007, p. 35; ACIA 2005, p. 418). A continuation of warm summers may 
lead to more and different predators, parasites, and pathogens. 
Northward expansion of Low Arctic and possibly sub-Arctic breeding 
shorebirds may lead to interspecific competition for an increasingly 
limited supply of suitable nesting habitat (Meltofte et al. 2007, p. 
    It is unlikely that any major changes in the extent of Calidris 
canutus breeding habitat have occurred to date, but long-term changes 
in breeding habitat resulting from climate change are likely to 
negatively affect this species in the future (COSEWIC 2007, p. 16). 
Using two early-generation climate models and two different climate 
scenarios (temperature increases of 3 and 9 [deg]F (1.7 and 5 [deg]C)), 
Z[ouml]ckler and Lysenko (2000, pp. iii, 8) predicted 16 to 33 percent 
loss of breeding habitat across all Calidris canutus subspecies by 2070 
to 2099. Some authors (Meltofte et al. 2007, p. 36; Piersma and 
Lindstr[ouml]m 2004, p. 66) have suggested that the 16 to 33 percent 
prediction is low, in part because it does not reflect ecological 
changes beyond outright loss of tundra. In 2007, COSEWIC concluded 
that, as the High Arctic zone is expected to shift north, C. canutus is 
likely to be among the species most affected. This would be the case 
particularly for populations breeding toward the southern part of the 
High Arctic zone, such as the rufa subspecies breeding in the central 
Canadian Arctic (COSEWIC 2007, p. 40), as such areas would be the first 
converted from tundra vegetation to shrubs and trees.
    Using multiple, recent-generation climate models and three 
emissions scenarios, Feng et al. (2012, p. 1366) found that tundra in 
northern Canada would be pushed poleward to the coast of the Arctic 
Ocean and adjacent islands and would be replaced by boreal forests and 
shrubs by 2040 to 2059. By 2080 to 2099, the tundra would be restricted 
to the islands of the Arctic Ocean, with total loss of tundra in some 
current red knot breeding areas (e.g., Southampton Island) (Feng et al. 
2012, p. 1366). The findings of Feng et al. (2012, p. 1366) support 
previous mapping by ACIA (2005, p. 991) that shows the treeline 
migrating north to overlap with the southern end of the red knot 
breeding range, including Southampton Island, by 2100.
    Vegetation changes may go beyond the replacement of tundra by 
forest and include the northward migration of vegetative subtypes 
within the remaining tundra zone. While predictions show forest 

[[Page 60049]]

limited to the southern end of the red knot's current breeding range by 
2100, migration of tundra subtypes may be widespread across the 
breeding range. A simulation by Kaplan et al. (2003, p. 10) showed that 
the current vegetative community (prostrate dwarf-shrub tundra) would 
be replaced by taller, denser vegetative communities throughout the 
entire known and potential breeding range by 2090 to 2100. The 
prostrate dwarf-shrub tundra would migrate north beyond the current 
breeding range of Calidris canutus rufa into the range of C.c. 
islandica, where it would replace the current community of cushion 
forb, lichen, and moss tundra (Kaplan et al. 2003, p. 10). This 
simulation was not intended as a realistic forward projection and did 
not include the potentially significant feedbacks between land surface 
and atmosphere. Instead, the simulation was meant to show one possible 
course of vegetative change and illustrate the sensitivity of arctic 
ecosystems to climate change (Kaplan et al. 2003, p. 2). However, such 
changes in the Arctic may already be under way, as several studies have 
found increased shrub abundance, biomass, and cover; increased plant 
canopy heights; and decreased prevalence of bare ground (Elmendorf et 
al. 2012a, p. 1; Elmendorf et al. 2012b; Myers-Smith et al. 2011, p. 2; 
Walker et al. in Richter-Menge et al. 2011, p. 93).
Arctic Warming--Summary
    Arctic regions are warming much faster than the global average 
rates, and the Canadian Archipelago is predicted to experience some of 
the fastest warming in the Arctic. Red knots currently breed in a 
region of sparse, low tundra vegetation within the southern part of the 
High Arctic and the northern limits of the Low Arctic. Forests are 
expected to colonize the southern part of the red knot's current 
breeding range by 2100, and vegetation throughout the entire breeding 
range may become taller and denser and with less bare ground, 
potentially making it unsuitable for red knot nesting. These changes 
may be accelerated near coastlines, where red knots breed, due to the 
loss of sea ice that currently cools the adjacent land. Loss of sea ice 
may also make the central Canadian island habitats more maritime-
dominated and, therefore, less suitable for breeding shorebirds. The 
red knot's breeding range may also experience changes in freshwater 
wetland foraging habitats, as well as unpredictable but profound 
ecosystem changes (e.g., interactions among predators, prey, and 
competitors). The red knot's adaptive capacity to withstand these 
changes in place, or to shift its breeding range northward, is unknown 
(also see Factor B, and Cumulative Effects, below).
Factor A--Conservation Efforts
    We are unaware of any broad-scale conservation measures to reduce 
the threat of destruction, modification, or curtailment of the red 
knot's habitat or range. Specifically, no conservation measures are 
specifically aimed at reducing sea level rise or warming conditions in 
the Arctic. As described in the sections above, shorebird reserves have 
been established at several key red knot sites in South America, and 
regional efforts are in progress to develop and implement urban 
development plans to help protect red knot habitats at some of these 
sites. In the United States, the Service is working with partners to 
minimize the effects of shoreline stabilization on shorebirds and other 
beach species (e.g., Rice 2009, entire), and there are efforts in 
Delaware Bay to maintain horseshoe crab spawning habitat (and, 
therefore, red knot foraging habitat) via beach nourishment (e.g., 
Niles et al. 2013, entire; USACE 2012, entire; Kalasz 2008, entire). In 
addition, local or regional efforts are ongoing to control several 
species of invasive beach vegetation. While additional best management 
practices could be implemented to address shoreline development and 
stabilization, beach cleaning, invasive species, agriculture, and 
aquaculture, we do not have any information that specific, large-scale 
actions are being taken to address these concerns such that those 
efforts would benefit red knot populations or the subspecies as a 
whole. See the supplemental document ``Factor D: Inadequacies of 
Existing Regulatory Mechanisms'' regarding regulatory mechanisms 
relevant to coastal development, shoreline stabilization, beach 
cleaning, and invasive species.
Factor A--Summary
    Within the nonbreeding portion of the range, red knot habitat is 
primarily threatened by the highly interrelated effects of sea level 
rise, shoreline stabilization, and coastal development. The primary red 
knot foraging habitats, intertidal flats and sandy beaches, will likely 
be locally or regionally inundated as sea levels rise, but replacement 
habitats are likely to re-form along eroding shorelines in their new 
positions. However, if shorelines experience a decades-long period of 
rapid sea level rise, high instability, and landward migration, the 
formation rate of new foraging habitats may be slower than the 
inundation rate of existing habitats. In addition, low-lying and narrow 
islands (e.g., in the Caribbean, along the Gulf and Atlantic coasts) 
may disintegrate rather than migrate, representing a net loss of red 
knot habitat.
    Superimposed on changes from sea level rise are widespread human 
efforts to stabilize the shoreline, which are known to exacerbate 
losses of intertidal habitats by blocking their landward migration. 
About 40 percent of the U.S. coastline within the range of the red knot 
is already developed, and much of this developed area is stabilized by 
a combination of existing hard structures and ongoing beach nourishment 
programs. Hard stabilization structures and dredging degrade and often 
eliminate existing red knot habitats, and in many cases prevent the 
formation of new shorebird habitats. Beach nourishment may temporarily 
maintain suboptimal shorebird habitats where they would otherwise be 
lost as a result of hard structures, but beach nourishment also has 
adverse effects to red knots and their habitats. In those times and 
places where artificial beach maintenance is abandoned, the remaining 
alternatives available to coastal communities would likely be limited 
to either a retreat from the coast or increased use of hard structures 
to protect development. The quantity of red knot habitat would be 
markedly decreased by a proliferation of hard structures. Red knot 
habitat would be significantly increased by retreat, but only where 
hard stabilization structures do not exist or where they get 
dismantled. Relative to the United States, little is known about 
development-related threats to red knot nonbreeding habitat in other 
countries. However, in some key international wintering and stopover 
sites, development pressures are likely to exacerbate habitat impacts 
caused by sea level rise.
    Lesser threats to nonbreeding habitat include beach cleaning, 
invasive vegetation, agriculture, and aquaculture. The practice of 
intensive beach raking may cause physical changes to beaches that 
degrade their suitability as red knot habitat. Although not a primary 
cause of habitat loss, invasive vegetation can be a regionally 
important contributor to the overall loss and degradation of the red 
knot's nonbreeding habitat. Agriculture and aquaculture are a minor but 
locally important contributor to overall loss and degradation of the 
red knot's nonbreeding habitat, particularly for moderate numbers of 
red knots that winter or stopover in Northeast Brazil where habitats 
were likely impacted by

[[Page 60050]]

the rapid expansion of shrimp farming since 1998.
    Within the breeding portion of the range, the primary threat to red 
knot habitat is from climate change. With arctic warming, vegetation 
conditions on the breeding grounds are expected to change, causing the 
zone of nesting habitat to shift north and perhaps contract. These 
effects may be exacerbated by loss of sea ice. Arctic freshwater 
systems, foraging areas for red knots during the nesting season, are 
particularly sensitive to climate change. Unpredictable but profound 
ecosystem changes (e.g., interactions among predators, prey, and 
competitors) may also occur.
    Threats to the red knot from habitat destruction and modification 
are occurring throughout the entire range of the subspecies. These 
threats include climate change, shoreline stabilization, and coastal 
development, exacerbated regionally or locally by lesser habitat-
related threats such as beach cleaning, invasive vegetation, 
agriculture, and aquaculture. The subspecies-level impacts from these 
activities are expected to continue into the future.
Factor B. Overutilization for Commercial, Recreational, Scientific, or 
Educational Purposes
    In this section, we discuss historic shorebird hunting in the 
United States that caused a substantial red knot population decline, 
ongoing shorebird hunting in parts of the Caribbean and South America, 
and potential effects to red knots from scientific study.
Factor B--Hunting
    Since the late 19th century, hunters concerned about the future of 
wildlife and the outdoor tradition have made countless contributions to 
conservation. In many cases, managed hunting is an important tool for 
wildlife management. However, unregulated or illegal hunting can cause 
population declines, as was documented in the 1800s for red knots in 
the United States. While no longer a concern in the United States, 
underregulated or illegal hunting of red knots and other shorebirds is 
ongoing in parts of the Caribbean and South America.
Hunting--United States (Historical)
    Red knots were heavily hunted for both market and sport during the 
19th and early 20th centuries (Harrington 2001, p. 22) in the Northeast 
and the mid-Atlantic. Red knot population declines were noted by 
several authors of the day, whose writings recorded a period of 
intensive hunting followed by the introduction of regulations and at 
least partial population recovery. As early as 1829, Wilson (1829, p. 
140) described the red knot as a favorite among hunters and bringing a 
good market price. Giraud (1844, p. 225) described red knot hunting in 
the South Bay of Long Island. Noting confusion over species common 
names, Roosevelt (1866, pp. 91-96) reported that hunting of ``bay 
snipe'' (a name applied to several shorebird species including red 
knot) primarily occurred from Cape Cod to New Jersey, rarely south of 
Virginia. Specific to red knots, Roosevelt (1866, p. 151) noted they 
were ``killed indiscriminately . . . with the other bay-birds.'' 
Hinting at shorebird population declines, Roosevelt (1866, pp. 95-96) 
found that ``the sport [of bay snipe shooting] has greatly diminished 
of late . . . a few years ago . . . it was no unusual thing to expend 
twenty-five pounds of shot in a day, where now the sportsman that could 
use up five would be fortunate.''
    Mackay (1893, p. 29) described a practice on Cape Cod during the 
1850s called ``fire-lighting,'' involving night-time hand-harvest via 
lantern light. In just one instance, ``six barrels'' of red knots taken 
by fire-lighting were shipped to Boston (Mackay 1893, p. 29). Fire-
lighting continued ``several years'' before it was banned (Mackay 1893, 
p. 29). Red knots continued to be taken ``in large numbers on the 
Atlantic seaboard (Virginia) . . . one such place shipping to New York 
City in a single spring, from April 1 to June 3, upwards of six 
thousand Plover, a large share of which were Knots'' (Mackay 1893, p. 
30). Mackay (1893, p. 30) concluded that red knots were ``in great 
danger of extinction.''
    Shriner (1897, p. 94) reported, ``This bird was formerly very 
plentiful in migrations in New Jersey, but it has been killed off to a 
great extent, proving an easy prey for pothunters,'' and Eaton (1910, 
p. 94) described red knots as ``much less common than formerly.'' 
Echoing Mackay (1893), Forbush (1912, pp. 262-266) cited numerous 
sources in describing a substantial coastwide decline in red knot 
numbers, and concluded, ``The decrease is probably due . . . to 
shooting both spring and fall all along our coasts, and possibly to 
some extent in South America . . . its extirpation from the Atlantic 
coast of North America is [possible] in the near future.''
    By 1927, Bent (1927, p. 132) noted signs of red knot population 
recovery, ``Excessive shooting, both in spring and fall reduced this 
species to a pitiful remnant of its former numbers; but spring shooting 
was stopped before it was too late and afterwards this bird was wisely 
taken off the list of game birds; it has increased slowly since then, 
but is far from abundant now.'' Urner and Storer (1949, pp. 192-193) 
reached the same conclusion, and documented population increases along 
New Jersey's Atlantic coast from 1931 to 1938. Based on his bird 
studies of Cape May, New Jersey, Stone (1937, p. 465) concluded that 
the red knot population decline had not been as sharp as previously 
thought, and that ``since the abolishing of the shooting of shore birds 
it has steadily increased in abundance.'' It is unclear whether the red 
knot population fully recovered its historical numbers (Harrington 
2001, p. 22) following the period of unregulated hunting, and it is 
possible this episode reduced the species' resilience to face other 
threats that emerged over the course of the 20th century. However, 
legal hunting of red knots is no longer allowed in the United States, 
and there is no indication of illegal hunting from any part of its 
mainland U.S. range.
Hunting--Caribbean and South America (Current)
    Both legal and illegal sport and subsistence hunting of shorebirds 
takes place in several known red knot wintering and migration stopover 
areas. This analysis focuses on areas where both red knots and hunting 
are known to occur, although in many areas we lack specific information 
regarding levels of red knot mortality from hunting. Therefore, we 
document the activity and explain that red knots could be affected, but 
draw no conclusions about direct mortality unless specifically noted.
    Moving from north to south, hunting is known from the Bahamas, 
including Andros, but it is not known if shorebirds specifically are 
hunted (B. Andres pers. comm. December 21, 2011); red knot hunting is 
prohibited by law (see supplemental document--Factor D). Likewise, 
hunting is considered a general threat to birds in Cuba but no specific 
information is available (B. Andres pers. comm. December 21, 2011). 
Regulated sport hunting occurs in Jamaica, but red knots are among the 
protected bird species for which hunting is prohibited in that 
country's wildlife law. Hunting occurs in Haiti, but information is not 
available specific to shorebirds (B. Andres pers. comm. December 21, 
2011). U.S. laws including the Endangered Species Act (regulating take 
of listed species) and the Migratory Bird Treaty Act (MBTA) (regulating 
harvest of migratory birds) apply in Puerto Rico and the U.S. Virgin 
Islands. In Puerto Rico, hunting is strictly regulated and permitted 
only for

[[Page 60051]]

certain species, but enforcement is lacking and nonlicensed hunters 
outnumber legal hunters. In the U.S. Virgin Islands, unregulated legal 
hunting, as well as poaching, has extirpated the West Indian whistling-
duck (Dendrocygna arborea) (B. Andres pers. comm. December 21, 2011). 
General enforcement of hunting regulations is lacking in the U.S. 
Virgin Islands, but shorebird hunting is negligible (B. Andres pers. 
comm. February 5, 2013 and December 21, 2011).
    Hunting birds is popular in Trinidad and Tobago. Seabird colonies 
are threatened by poachers who collect the adult birds for meat and 
presumably also take the eggs. In addition to seabirds, species at 
particular risk from hunting include several species of wading birds, 
fowl, and waterfowl (B. Andres pers. comm. December 21, 2011). Although 
hunters generally target larger waterbirds, harvest is a threat to 
shorebirds as well. There are about 750 hunters (on both Trinidad and 
Tobago), the season ranges from November to February, and there are no 
bag limits (USFWS 2011e, p. 4). Red knot hunting is prohibited by law 
in Belize and Uruguay.
Current Hunting--Lesser Antilles Shooting Swamps
    In parts of the Lesser Antilles, legal sport hunters target 
shorebirds in ``shooting swamps.'' Most of the migratory shorebird 
species breeding in eastern North America and the Arctic pass through 
the Caribbean during late August and September on their way to 
wintering areas. When they encounter severe storms during migration, 
the birds use the islands as refuges before moving on to their final 
destinations. Hunting clubs take advantage of these events to shoot 
large numbers of shorebirds at one time (Nebel 2011, p. 217).
Lesser Antilles--Barbados
    Barbados has a tradition of legal shorebird hunting that began with 
the colonists in the 17th and 18th centuries. The current shooting 
swamps were artificially created and can attract large numbers of 
migrant shorebirds during inclement weather. The open season for 
shorebirds is July 15 to October 15, and there is no daily bag limit. 
Several species are protected, and hunters have voluntarily agreed to 
stop the harvest of red knots. Work is in progress to gather current 
mortality levels and develop a model of sustainable shorebird harvest. 
To date, half of the shooting swamps on Barbados have agreed to furnish 
harvest data (USFWS 2011e, p. 2). As of 1991, Hutt (pp. 77-78) 
estimated that fewer than 100 hunters killed 15,000 to 20,000 
shorebirds per year at 7 major shooting swamps. Although conservation 
progress has been made, the number of shorebirds killed annually is 
still around 26,000. Hunters have a partial agreement with the 
conservation community to lower the annual shorebirds harvest to 22,500 
(Eubanks 2011).
    Although hunting pressure on shorebirds remains high, red knots 
have not been documented in Barbados in large numbers. The red knot is 
a regular fall transient, usually occurring as single individuals and 
in small groups in late August and early September, and typically 
utilizing coastal swamps during adverse weather (Hutt and Hutt 1992, p. 
70; Hutt 1991, p. 89). Detailed records from 1950 to 1965 show an 
average of about 20 red knots per year. Red knots may occur very 
exceptionally in flocks of up to a dozen birds; a record of 63 birds--
brought in by a storm--were shot in 1 day in 1951 (Hutt and Hutt 1992, 
p. 70). From 1990 to 1992, seven shooting swamps were active, and red 
knot mortality was reported from two of the swamps; nine red knots were 
shot at Best Pond, and one was shot at Woodbourne. Due to its coastal 
location, Best Pond attracted more red knots than other shooting 
swamps, but it has been closed to hunting due to residential 
development (W. Burke pers. comm. October 12, 2011), and Woodbourne has 
been restored as a ``no-shoot'' shorebird refuge (BirdLife 
International 2009; Burke 2009, p. 287). The remaining shooting swamps 
in Barbados no longer target red knots, and only a few knots have been 
observed in recent years (W. Burke pers. comm. October 12, 2011).
Lesser Antilles--French West Indies
    The French West Indies consist of Guadeloupe and its dependencies, 
Martinique, Saint Martin, and Saint Barth[eacute]lemy. To date, red 
knots have been reported only from Guadeloupe (eBird.org 2012).
    Like Barbados, legal sport hunting of shorebirds has a long 
tradition on the French territories of Guadeloupe and Martinique (USFWS 
2011e, p. 3). Wetlands are not managed for shorebird hunting in 
Guadeloupe, but are sometimes on Martinique (USFWS 2011e, p. 3). 
However, Guadeloupe has several isolated mangrove swamps that serve to 
concentrate shorebirds for shooting (Nebel 2011, p. 217). Approximately 
1,400 hunters on Martinique and 3,000 hunters on Guadeloupe harvest 14 
to 15 shorebird species, which are typically eaten. The hunting season 
runs from July to January, and no daily bag limits are set. The 
shorebird hunting pressure in the French West Indies may be greater 
than on Barbados. There are no reliable estimates for the magnitude of 
the harvest; however, a single hunter has been known to harvest 500 to 
1,000 shorebirds per season. Work is ongoing to more accurately 
determine the magnitude of the shorebird harvest in the French West 
Indies (USFWS 2011e, p. 3).
    Although shorebird hunting has been previously documented on 
Guadeloupe (USFWS 2011e, p. 3), the issue gained notoriety in September 
2011 when two whimbrels (Numenius phaeopus), fitted with satellite 
transmitters as part of a 4-year tracking study, were killed by 
hunters. The 2 birds were the first of 17 tracked whimbrels to stop on 
Guadeloupe; they were not migrating together, but both stopped on the 
island after encountering different storm systems. As both whimbrels 
were shot in a known shooting swamp within hours of arriving on 
Guadeloupe, the circumstances of these two documented mortalities 
suggest that shorebird hunting pressure may be very high (Smith et al. 
2011b). Like other overseas territories, Guadeloupe is not covered by 
key European laws for biodiversity conservation (Nebel 2011, p. 217). 
Following the shooting of the tracked whimbrels, conservation groups 
launched an appeal for the protection of birds and their habitats in 
French overseas departments in the Caribbean and elsewhere (Nebel 2011, 
p. 217). The French Government has recently acted to impose new 
protective measures in Guadeloupe. The National Hunting and Wildlife 
Agency has begun negotiating bag limits and is working on a new 
regulation that would stop hunting for 5 days following a tropical 
storm warning, but these measures are not yet in effect (A. Levesque 
pers. comm. January 8, 2013; Niles 2012c). Significantly, the red knot 
was recently added to the list of protected species, and hunter 
education about red knots is in progress (A. Levesque pers. comm. 
January 8, 2013; Niles 2012c).
    Although the red knot was (until recently) listed as a game bird, 
mortality from hunting was probably low because red knots occur only in 
small numbers. In Guadeloupe, the red knot is an uncommon but regular 
visitor during fall migration, typically in groups of 1 to 3 birds, but 
as many as 16 have been observed in 1 flock. Probably no more than a 
few dozen red knots were shot per year in Guadeloupe (A. Levesque pers. 
comm. October 11, 2011), prior to its protected designation.

[[Page 60052]]

Current Hunting--The Guianas
    Band recoveries indicate that red knots are killed commonly for 
food in some regions of South America, especially in the Guianas (i.e., 
Suriname, Guyana, and French Guiana). The overall take from these 
activities is unknown, but the number of band recoveries (about 17) in 
the Guianas hints that the take may be substantial (Harrington 2001, p. 
22). More recently two additional bands were recovered from red knots 
shot in French Guiana (D. Mizrahi pers. comm. October 16, 2011). One of 
these birds, shot in a rice field near Mana in May 2011, was banded in 
Delaware Bay in May 2005 and was subsequently resighted over 30 times 
in New Jersey, Delaware, and Florida (J. Parvin pers. comm. September 
12, 2011).
    Rice fields and other impoundments are prevalent in French Guiana 
and Guyana (USFWS 2011e, p. 3). In the rice fields near Mana, French 
Guiana, more than 1,700 red knots were observed in late August 2012 
(Niles 2012b). During the same timeframe, about 30 new shotgun shells 
per kilometer were collected along the dikes around the fields. This 
estimated density of spent shotgun shells is a minimum as some of the 
dikes were swept by the tides and most were overgrown with vegetation, 
limiting detectability. In addition to observing the indirect evidence 
of hunting, researchers saw two people with guns during 4 days in the 
field (Niles 2012b). Shorebirds are harvested legally in French Guiana 
and Guyana, although the magnitude of the harvest is unknown (USFWS 
2011e, p. 3). Shorebird hunting is unregulated in French Guiana (A. 
Levesque pers. comm. January 8, 2013; D. Mizrahi pers. comm. October 
16, 2011), which is an overseas region of France.
    Harvest of any shorebirds has been illegal in Suriname since 2002, 
but there is little enforcement. Law enforcement is hampered by limited 
resources (e.g., working boats, gasoline), and several tens of 
thousands of shorebirds are trapped and shot each year. A 2006 survey 
indicated that virtually all shorebird species occurring in Suriname 
were illegally hunted and trapped in some quantity, with the lesser 
yellowlegs (Tringa flavipes) and semipalmated sandpiper (Calidris 
pusilla) being the dominant species. The survey also documented an 
illegal food trade of shorebirds, including selling to local markets. 
Shorebirds are harvested by shooting, netting, and using choke wires. 
Many shorebirds are taken by Guyanese fishermen working in Suriname. 
The Suriname coast is mainly mudflats and much of the coast is legally 
protected. Three coastal areas in Suriname are designated as sites of 
hemispheric importance by WHSRN, and it is likely that hunting occurs 
in at least two of them. Education and awareness programs have begun 
along the coast of Suriname, and a hunter training program is being 
developed (USFWS 2011e, p. 3).
    Red knots are primarily passage migrants in the Guyanas, with many 
more birds documented in French Guiana (Niles 2012b) than in Suriname, 
where the habitat is not ideal for red knots (B. Harrington pers. comm. 
March 31, 2006; Spaans 1978, p. 72). Based on work in Suriname and 
French Guiana since 2008, D. Mizrahi (pers. comm. October 16, 2011) 
suspects that red knot mortality from hunting in these countries may be 
an order of magnitude higher than in Guadeloupe, given the much larger 
stopover populations (i.e., hundreds of birds) that have been observed 
in the Guianas. As described under Species Information above, red knots 
and other shorebirds are known to segregate by sex during migration. 
The effects of hunting would be far greater if mortality 
disproportionately affects adult females (D. Mizrahi pers. comm. 
October 16, 2011), which may predominate red knot aggregations at 
certain times of the year.
Current Hunting--Brazil
    Hunting migratory shorebirds for food was previously common among 
local communities in Maranh[atilde]o, Brazil. Shorebirds provided an 
alternative source of protein, and birds like the red knot with high 
subcutaneous fat content for long migratory flights were particularly 
valued. According to local people, red knot was among the most consumed 
species, although no data are available to document the number of birds 
taken. Local people say that, although some shorebirds are still 
hunted, this practice has greatly decreased over the past decade, and 
hunting is not thought to amount to a serious cause of mortality (Niles 
et al. 2008, p. 99). Outside the State of Maranh[atilde]o, hunting 
pressure on red knots has not been characterized. For some bird 
species, unregulated subsistence hunting in Brazil may be causing 
species declines (R. Huffines pers. comm. September 13, 2011).
    Commercial and recreational hunting are prohibited in all Brazilian 
territory, except for the state of Rio Grande do Sul, which includes 
the Logoa do Peixe stopover site. The Rio Grande do Sul hunting law 
provides a list of animals that can be hunted, prohibits trapping, and 
bans commercialized hunting (B. Andres pers. comm. December 21, 2011). 
Poaching is known from waterbird colonies in Brazil (B. Andres pers. 
comm. December 21, 2011), but no information is available regarding any 
illegal shorebird harvest.
Factor B--Scientific Study
    About 1,000 red knots per year are trapped for scientific study in 
Delaware Bay, and about 300 in South America (Niles et al. 2008, p. 
100). In some years, additional birds are trapped in other parts of the 
range (e.g., Newstead et al. in press; Schwarzer et al. 2012, p. 728; 
Baker et al. 2005, p. 13). In an effort to further understand the red 
knot's rates of weight gain, migratory movements, survival rates, and 
conservation needs, the trapped birds are weighed and measured, leg-
banded, and fitted with individually numbered color-flags. In some 
years, coordinated tissue sampling (e.g., feathers, blood, mouth swabs) 
is conducted for various scientific studies (Niles et al. 2008, p. 
100), such as contaminants testing, stable isotope analysis, or genetic 
research. Prolonged captivity or excessive handling during these 
banding operations can cause Calidris canutus to rapidly lose weight, 
about 0.04 ounces (oz) (1 gram (g)) per hour (L. Niles and H. Sitters 
pers. comm. September 4, 2008; Davidson 1984, p. 1724). In rare 
circumstances, C. canutus held in captivity during banding, especially 
when temperatures are high, can develop muscle cramps that can be fatal 
or leave birds vulnerable to predators (Rogers et al. 2004, p. 157).
    Through 2008, about 50 of the birds caught in Delaware Bay each 
year were the subject of radiotelemetry studies in which a 0.1-oz (2-g) 
radio tag was glued to the back of each bird (Niles et al. 2008, p. 
100). Additional birds were recently radio-tracked in Texas (Newstead 
pers. comm. August 20, 2012). The tags are expected to drop off after 1 
to 2 months through the natural replacement of skin. Resighting studies 
in subsequent years showed that the annual survival of radio-tagged 
birds was no different from that of birds that had only been banded 
(Niles et al. 2008, p. 100). In more recent years, tens of red knots 
have been fitted with geolocators. After 1 year, researchers found no 
significant differences in the resighting rates of birds carrying 
geolocators, suggesting that these devices did not affect survival 
(Niles et al. 2010a, p. 123).
    Considerable care is taken to minimize disturbance caused to 
shorebirds from these research activities. Numbers of birds per catch 
and total numbers caught over the

[[Page 60053]]

season are limited, and careful handling protocols are followed, 
including a 3-hour limit on holding times (Niles et al. 2010a, p. 124; 
L. Niles and H. Sitters pers. comm. September 4, 2008; Niles et al. 
2008). Despite these measures, hundreds of red knots are temporarily 
stressed during the course of annual research, and mortality, though 
rare, does occasionally occur (K. Clark pers. comm. January 21, 2013; 
Taylor 1981, p. 241). However, we conclude that these research 
activities are not a threat to the red knot because evaluations have 
shown no effects of these short-term stresses on red knot survival. 
Further, the rare, carefully documented, and properly permitted 
mortality of an individual bird in the course of well-founded research 
does not affect red knot populations or the overall subspecies.
Factor B--Conservation Efforts
    As discussed above, a few countries where shorebird hunting is 
legal have implemented voluntary restrictions on red knot hunting, 
increased hunter education efforts, established ``no-shoot'' shorebird 
refuges, and are developing models of sustainable harvest. Ongoing 
scientific research has benefitted red knot conservation in general 
and, through leg-band recoveries, has provided documentation of 
hunting-related mortality. Research activities adhere to best practices 
for the careful capture and handling of red knots.
Factor B--Summary
    Legal and illegal sport and market hunting in the mid-Atlantic and 
Northeast United States substantially reduced red knot populations in 
the 1800s, and we do not know if the subspecies ever fully recovered 
its former abundance or distribution. Neither legal nor illegal hunting 
are currently a threat to red knots in the United States, but both 
occur in the Caribbean and parts of South America. Hunting pressure on 
red knots and other shorebirds in the northern Caribbean and on 
Trinidad is unknown. Hunting pressure on shorebirds in the Lesser 
Antilles (e.g., Barbados, Guadeloupe) is very high, but only small 
numbers of red knots have been documented on these islands, so past 
mortality may not have exceeded tens of birds per year. Red knots are 
no longer being targeted in Barbados or Guadeloupe, and other measures 
to regulate shorebird hunting on these islands are being negotiated. 
Much larger numbers (thousands) of red knots occur in the Guianas, 
where legal and illegal subsistence shorebird hunting is common. About 
20 red knot mortalities have been documented in the Guianas, but total 
red knot hunting mortality in this region cannot be surmised. 
Subsistence shorebird hunting was also common in northern Brazil, but 
has decreased in recent decades. We have no evidence that hunting was a 
driving factor in red knot population declines in the 2000s, or that 
hunting pressure is increasing. In addition, catch limits, handling 
protocols, and studies on the effects of research activities on 
survival all indicate that overutilization for scientific purposes is 
not a threat to the red knot.
    Threats to the red knot from overutilization for commercial, 
recreational, scientific, or educational purposes exist in parts of the 
Caribbean and South America. Specifically, legal and illegal hunting 
does occur. While red knot mortality is documented, we have no 
information to suggest that mortality levels are high enough to affect 
red knot populations or the subspecies as a whole. We expect mortality 
of individual knots from hunting to continue into the future, but at 
stable or decreasing levels due to the recent international attention 
to shorebird hunting.
Factor C. Disease or Predation
    Red knots are exposed to several diseases and experience variable 
rates of predation from avian and mammalian predators throughout their 
range. In this section, we discuss known parasites and viruses, and the 
direct and indirect effects of predation in the red knot's breeding, 
wintering, and migration areas.
Factor C--Disease
    Red knots are exposed to parasites and disease throughout their 
annual cycle. Susceptibility to disease may be higher when the energy 
demands of migration have weakened the immune system. Studying red 
knots in Delaware Bay in 2007, Buehler et al. (2010, p. 394) found that 
several indices of immune function were lower in birds recovering 
protein after migration than in birds storing fat to fuel the next leg 
of the migration. These authors hypothesized that fueling birds may 
have an increased rate of infection or may be bolstering immune 
defense, or recovering birds may be immuno-compromised because of the 
physical strain of migratory flight or as a result of adaptive energy 
tradeoffs between immune function and migration, or both (Buehler et 
al. 2010, p. 394). A number of known parasites and viruses are 
described below, but we have no evidence that disease is a current 
threat to the red knot.
    An epizootic disease (epidemic simultaneously affecting many 
animals) that caused illness or death of about 150 red knots on the 
west coast of Florida in December 1973 and November 1974 was caused by 
a protozoan (single-celled organism) parasite, most likely an 
undescribed sporozoan (reproducing by spores) species (USFWS 2003, p. 
22; Harrington 2001, p. 21, Woodward et al. 1977, p. 338).
    On April 7, 1997, 26 red knots, 10 white-rumped sandpipers 
(Calidris fuscicollis), and 3 sanderlings (Calidris alba) were found 
dead or dying along 6.2 mi (10 km) of beach at Lagoa do Peixe in 
southern Brazil. The following day, another 13 dead or sick red knots 
were found along 21.7 mi (35 km) of nearby beach (Niles et al. 2008, p. 
101; Baker et al. 1998, p. 74). All 35 red knots were heavily infected 
with hookworms (Phylum Acanthocephala), which punctured their 
intestines. Although hookworms can cause sudden deaths in birds, the 
lungs of some birds were discolored, suggesting there may have been an 
additional factor in their mortality. Three white-rumped sandpipers and 
three sanderlings were also examined, and none appeared to be infected 
with hookworms, again suggesting another cause of death. Bacterial 
agents and environmental contaminants were not ruled out (Baker et al. 
1998, p. 75), but Harrington (2001, p. 21) attributed the deaths to the 
hookworms. Smaller mortalities of spring migrants with similar symptoms 
were also reported from Uruguay in the 2000s (Niles et al. 2008, p. 
    Blood parasites represent a complex, spatially heterogeneous host-
parasite system having ecological and evolutionary impacts on host 
populations. Three closely related genera, (Plasmodium, Haemoproteus 
and Leucocytozoon) are commonly found in wild birds, and infections in 
highly susceptible species or age classes may result in death (D'Amico 
et al. 2008, p. 195). Reported red knot mortalities in Florida in 1981 
were attributed to the blood parasite Plasmodium hermani (Niles et al. 
2008, p. 101; Harrington 2001, p. 21). However, no blood parasites 
(Plasmodium, Haemoproteus or Leucocytozoon spp.) were found in red 
knots sampled in 2004 and 2005 in Tierra del Fuego (181 samples), 
Maranh[atilde]o, Brazil (52 samples), or Delaware Bay (140 samples), 
and this finding is consistent with the generally low incidence of 
blood parasite vectors along marine shores (D'Amico et al. 2008, pp. 
193, 197). No blood parasites

[[Page 60054]]

(Plasmodium or Haemoproteus spp.) were detected in 156 red knots 
sampled at 2 sites in Argentina (R[iacute]o Grande and San Antonio 
Oeste) in 2005 and 2006 (D'Amico et al. 2007, p. 794).
    In 2008, Escudero et al. (2012, pp. 362-363) observed a high 
prevalence of a Digenea parasitic flatworm (Bartolius pierrei) in clams 
(Darina solenoids), a major prey item of red knots foraging at 
R[iacute]o Grande in Argentinean Tierra del Fuego. Clams near the 
surface of the sediment were the most highly infected by the flatworm, 
and were preferentially eaten by red knots, probably due to their 
larger size. While digenean worm parasites may be part of the natural 
intestinal fauna of red knots, parasites are detrimental by definition. 
It is likely that the adult stage of this parasite living in the 
intestines and stomach causes either damage or an immunological 
response, adversely affecting the condition of the host birds (Escudero 
et al. 2012, p. 363). Farther north, at Fracasso Beach, 
Pen[iacute]nsula Vald[eacute]s, Argentina, Cremonte (2004, p. 1591) 
found that B. pierrei uses the clam Darina solenoides as its 
intermediate host. The red knot and a gull species (Family Laridae) act 
as definitive hosts, with 92 percent of red knots infected. Bartolius 
pierrei did not parasitize other invertebrates that share the 
intertidal habitat with D. solenoides, suggesting the parasite may be 
adapted to target red knot prey species. Bartolius pierrei is an 
endemic parasite of the Magellan region, distributed where its 
intermediate clam host is present, from San Jos[eacute] Gulf in 
Pen[iacute]nsula Vald[eacute]s to the southern tip of South America 
(Cremonte 2004, p. 1591). To date, the impacts of flatworm infection on 
red knot health or fitness have not been investigated.
    Ectoparasites, which live on the surface of the body, can affect 
birds by directly hindering their success in obtaining food and by 
acting as vectors and invertebrate hosts to microorganisms. For 
example, lice and mites infest skin and feathers leaving their hosts 
susceptible to secondary infections (D'Amico et al. 2008, p. 195). 
Individual red knots examined in 1968 (New York) and 1980 
(Massachusetts) were infested with bird lice (Mallophaga (Amblycera): 
Menoponidae), which live in the feather shafts. Based on the bird 
examined in 1980, the lice likely caused that red knot to molt some 
primary feathers, known as an adventitious molt. Other than the molt, 
this red knot appeared healthy (Taylor 1981, p. 241). In the course of 
ongoing field studies in Maranh[atilde]o, Brazil, all 38 knots caught 
and sampled in February 2005 were found to be heavily infected with 
ectoparasites. The birds were also extremely lightweight, less than the 
usual fat-free mass of red knots (Baker et al. 2005, p. 15). 
Fieldworkers have also noticed ectoparasites on a substantial number of 
red knots caught in Delaware Bay (Niles et al. 2008, p. 101).
    D'Amico et al. (2008, pp. 193, 197) examined red knots for 
ectoparasites at three sites in 2004 and 2005. All ectoparasites 
observed during this study were feather lice (Phthiraptera: Mallophaga 
(Amblycera)). Only 5 of 113 (4 percent) of red knots examined on Tierra 
del Fuego in R[iacute]o Grande, Argentina, had ectoparasites, while all 
36 knots (100 percent) examined in Maranh[atilde]o, Brazil, were 
infected. Almost 40 percent of the Brazilian birds had very high 
parasite loads. Of 256 red knots examined in Delaware Bay, 174 (68 
percent) had ectoparasites. Using feather isotopes from the Delaware 
Bay birds, D'Amico et al. (2008, p. 197) identified 90 of the 256 birds 
as coming from northern wintering areas (e.g., Brazil, the Southeast) 
and 66 from southern wintering areas (e.g., Tierra del Fuego) (the 
wintering region of the remaining 100 birds was unknown). The 
proportions of parasitized birds captured at Delaware Bay from the 
different wintering regions were not significantly different (50 
percent from northern areas infected versus 40 percent from southern 
areas). However, the northern-wintering red knots tended to have higher 
loads of ectoparasites (i.e., more parasites per bird). These data 
suggest that many southern birds may be infected during a short 
stopover during the northward migration or by direct contact in 
Delaware Bay (D'Amico et al. 2008, pp. 193, 197). To date, the impacts 
of ectoparasite infection on red knot health or fitness have not been 
    Associating characteristics of breeding and wintering habitats, 
chick energetics, and apparent immunocompetence (the ability of the 
body to produce a normal immune response following exposure to 
disease), Piersma (1997, p. 623) suggested that shorebird species make 
tradeoffs of immune system function versus growth and sustained 
exercise. This author suggested that these tradeoffs determine the use 
of particular habitat types by long-distance migrating shorebirds. Some 
species appear restricted to parasite-poor habitats such as the Arctic 
tundra and exposed seashores, where small investments in the immune 
system may suffice and even allow for high chick growth rates. However, 
such habitats are few and far between, necessitating long and demanding 
migratory flights and often high energy expenditures while in residence 
(e.g., to deal with cold temperatures) (Piersma 1997, p. 623). 
Increased adult survival afforded by inhabiting areas of low parasite 
loads may offset the energetic and other costs of breeding in the 
climatically marginal, but parasite-low, Arctic (USFWS 2003, p. 22). 
Piersma's (1997) parasite hypothesis predicts that red knots should 
evolve migrations to low-parasite marine wintering sites to reduce the 
fitness consequences of high ectoparasite loads in tropical Brazil, but 
there is likely a tradeoff with increased mortality for long-distance 
migration to cold-temperate Tierra del Fuego (D'Amico et al. 2008, p. 
    Species adapted to parasite-poor habitats may be particularly 
susceptible to parasites and pathogens (USFWS 2003, p. 22; Piersma 
1997, p. 623). For example, captive Calidris canutus are susceptible to 
common avian pathogens (e.g., the avian pox virus, bacterial 
infections, feather lice), and reconstructing a marine environment 
(i.e., flushing the cages with seawater) helps to reduce at least the 
external signs of infections (Piersma 1997, pp. 624-625).
    In summary, three localized red knot die-off events have been 
attributed to parasites, but these kinds of parasites (sporozoans, 
hookworms) have not been documented elsewhere or implicated in further 
red knot mortality. Blood parasites have caused red knot deaths, but 
blood parasite infections were not detected by testing that took place 
across the knot's geographic range in the 2000s. In contrast, flatworm 
infection is widespread in Argentina, and bird lice infection is 
widespread in tropical and temperate portions of the red knot's range. 
However, impacts of these infections on red knot health or fitness have 
not been documented. Red knots may be adapted to parasite-poor 
habitats, and may, therefore, be particularly susceptible to parasites 
and pathogens. However, we have no evidence that parasites have 
impacted red knot populations beyond causing normal, background levels 
of mortality, and we have no indications that parasite infection rates 
or fitness impacts are likely to increase. Therefore, we conclude 
parasites are not a threat to the red knot.
    Type A influenza viruses, also called avian influenza (AI), are 
categorized by two types of glycoproteins on their surface, abbreviated 
HA and NA (or H and N when given in various combinations to identify a 
unique type of AI virus). The AI viruses are also classified as high or 
low pathogenicity

[[Page 60055]]

(HPAI and LPAI). The term HPAI (high pathogenicity avian influenza) has 
a specific meaning relating to the ability of the virus to cause 
disease in experimentally inoculated chickens, and does not necessarily 
reflect the capacity of these viruses to produce disease in other 
species (Food and Agriculture Organization of the United Nations (FAO) 
2013). However, it is these more virulent (highly harmful or infective) 
HPAI viruses that cause outbreaks of sickness and death in humans and 
other species of mammals and birds (FAO 2013; Krauss et al. 2010, p. 
3373). Some LPAI types can mutate into HPAI forms (FAO 2013).
    Anseriformes (swans, geese, and ducks) and Charadriiformes (gulls 
and shorebirds) are the natural hosts of LPAI (FAO 2013; Maxted et al. 
2012, p. 322; Krauss et al. 2010, p. 3373; Olsen et al. 2006, p. 384). 
All 16 HA and 9 NA subtypes discovered to date have been detected in 
various combinations in wild aquatic birds, mainly LP forms. In 
general, LPAI viruses do not have significant health effects on wild 
birds, typically causing only a short-lived subclinical intestinal 
infection (FAO 2013; Krauss et al. 2010, p. 3373; Olsen et al. 2006, p. 
384). However, HPAI can also occur in wild birds. One form of HPAI 
(H5N1) has caused mortality in more than 60 wild bird species, with 
population-level impacts in a few of those species. Although numerous 
wild birds have become infected with H5N1, debate remains whether wild 
birds play a role in the geographic spread of the disease (Olsen et al. 
2006, pp. 387-388).
    Since 1985, AI surveillance has been conducted annually from mid-
May to early June in shorebirds and gulls in Delaware Bay. Influenza 
viruses (LP forms) are consistently isolated from shorebirds (i.e., the 
shorebirds were found to be carrying AI viruses) in Delaware Bay at an 
overall rate (5.2 percent) that is about 17 times higher than the 
combined rate of isolation at all other surveillance sites worldwide 
(0.3 percent) (Krauss et al. 2010, p. 3373). The isolation rate was 
even higher, 6.3 percent, from 2003 to 2008. Across global studies to 
date, AI viruses were rarely isolated from shorebirds except at two 
locations, Delaware Bay and a site in Australia (Krauss et al. 2010, p. 
3375). The convergence of host factors and environmental factors at 
Delaware Bay results in a unique ecological ``hot spot'' for AI viruses 
in shorebirds (Krauss et al. 2010, p. 3373). Among the Delaware Bay 
shorebird species, ruddy turnstones (Arenaria interpres) have the 
highest infection rates by far (Maxted et al. 2012, p. 323). Although 
overall AI rates in Delaware Bay shorebirds are very high, red knots 
are rarely infected (L. Niles and D. Stallknecht pers. comm. January 
25, 2013; Maxted et al. 2012, p. 322). Declining antibody prevalence in 
red knots over the stopover period suggests that their exposure to AI 
viruses generally occurs prior to arrival at Delaware Bay, with limited 
infection taking place at this site (Maxted et al. 2012, p. 322).
    In wild red knots in Delaware Bay, AI infection rates are low, and 
only LP forms have been detected (Maxted et al. 2012, pp. 322-323). 
There is no evidence that the LPAI documented in wild red knots causes 
any harm to the health of these birds (L. Niles and D. Stallknecht 
pers. comm. January 25, 2013). However, susceptibility of Calidris 
canutus to HP forms of influenza has been shown in captivity. Five of 
26 C. canutus islandica experimentally infected with an HPAI (H5N1) 
developed neurological disease or died during an experiment from 2007 
to 2009 (Reperant et al. 2011, pp. 1, 4, 8). The appearance of clinical 
signs in these birds was sudden and the affected birds did not behave 
significantly differently on the preceding days than birds that 
remained sub-clinically infected (Reperant et al. 2011, p. 4). See 
Cumulative Effects, below, for discussion of an unlikely but 
potentially high-impact interaction among AI, environmental 
contaminants, and climate change.
    Newcastle disease is a contagious bird disease (an avian 
paramyxovirus), and one of the most important poultry diseases 
worldwide. While people in direct contact with infected birds can get 
swelling and reddening of tissues around the eyes (conjunctivitis), no 
human cases of Newcastle disease have occurred from eating poultry 
products (Iowa State University 2008, entire). Although Newcastle 
disease is the most economically important, other types of avian 
paramyxovirus have been isolated from domestic poultry, where they 
occasionally cause respiratory and reproductive disease (Coffee et al. 
2010, p. 481). No information is available regarding health effects of 
avian paramyxovirus in shorebirds.
    From 2000 to 2005, Coffee et al. (2010, p. 481) tested 9,128 
shorebirds and gulls of 33 species captured in 10 U.S. States and 3 
countries in the Caribbean and South America for various types of avian 
paramyxovirus, including Newcastle disease virus. Avian paramyxoviruses 
were isolated from 60 (0.7 percent) samples, with 58 of the isolates 
coming from shorebirds (only 2 from gulls). All of the 58 positive 
shorebirds were sampled at Delaware Bay, and 45 of these isolates came 
from ruddy turnstones. The higher prevalence of avian paramyxovirus in 
ruddy turnstones mirrors the results observed for avian influenza 
viruses in shorebirds and may suggest similar modes of transmission 
(Coffee et al. 2010, p. 481). Of the birds sampled, 1,723 were red 
knots from Delaware Bay and 921 were red knots from other locations 
(Coffee et al. 2010, p. 483). Of these 2,644 red knots, only 7 tested 
positive (0.4 percent), and all 7 were captured in Delaware Bay (Coffee 
et al. 2010, p. 484). Like avian influenza virus, avian paramyxovirus 
infections in red knots may be site dependent, and at Delaware Bay 
these viruses may be locally amplified (Coffee et al. 2010, p. 486).
    Since 2002, migratory birds in Brazil have been tested for various 
viruses including West Nile and Newcastle. As of 2007, AI type H2 had 
been found in one red knot, equine encephalitis virus in another, and 
Mayaro virus in seven knots (Niles et al. 2008, p. 101). Evidence does 
not indicate that West Nile virus will affect red knot health, and 
shorebirds are generally not regarded as important avian hosts in West 
Nile virus epidemiology (D. Stallknecht pers. comm. January 25, 2013). 
In 2005 and 2006, 156 red knots were sampled at 2 sites in Argentina 
(R[iacute]o Grande and San Antonio Oeste) and tested for Newcastle 
disease virus, AI virus, and antibodies to the St. Louis encephalitis 
virus; all test results were negative (D'Amico et al. 2007, p. 794). 
One red knot was among 165 shorebirds of 11 species from southern 
Patagonia, Argentina, that were tested for all AI subtypes in 2004 and 
2005; no AI was detected (Escudero et al. 2008, pp. 494-495).
    For the most prevalent viruses found in shorebirds within the red 
knot's geographic range, infection rates in red knots are low, and 
health effects are minimal. We conclude that viral infections 
documented to date do not cause significant mortality and are not 
currently a threat to the red knot. However, see Cumulative Effects, 
below, regarding an unlikely but potentially high-impact, synergistic 
effect among avian influenza, environmental contaminants, and climate 
change in Delaware Bay.
Factor C--Predation
Predation--Nonbreeding Areas
    In wintering and migration areas, the most common predators of red 
knots are peregrine falcons (Falco peregrinus), harriers (Circus spp.), 
accipiters (Family Accipitridae), merlins (F. columbarius), shorteared 
owls (Asio flammeus), and

[[Page 60056]]

greater black-backed gulls (Larus marinus) (Niles et al. 2008, p. 28). 
In addition to greater black-backed gulls, other large gulls (e.g. 
herring gulls (Larus argentatus)) are anecdotally known to prey on 
shorebirds (Breese 2010, p. 3). Predation by a great horned owl (Bubo 
virginianus) has been documented in Florida (A. Schwarzer pers. comm. 
June 17, 2013). Nearly all documented predation of wintering red knots 
in Florida has been by avian, not terrestrial, predators (A. Schwarzer 
pers. comm. June 17, 2013). However in migration areas like Delaware 
Bay, terrestrial predators such as red foxes (Vulpes vulpes) and feral 
cats (Felis catus) may be a threat to red knots by causing disturbance, 
but direct mortality from these predators may be low (Niles et al. 
2008, p. 101).
    Ellis et al. (2002, pp. 316-317) summarized the documented prey 
species taken by peregrine falcons in Patagonia and Tierra del Fuego, 
based on early 1980s field surveys. Shorebirds represented only 8 of 55 
reported prey species (about 15 percent), but accounted for 44 of 138 
individual birds preyed on (about 32 percent) (Ellis et al. 2002, pp. 
316-317), suggesting that shorebirds may be a favored prey type. Red 
knots were not reported among the prey species, but these authors 
considered their list incomplete and believed many more prey species 
would be identified from further sampling (Ellis et al. 2002, pp. 317-
    Peregrine falcons have been seen frequently along beaches in Texas, 
where dunes would provide good cover for peregrines preying on red 
knots foraging along the narrow beachfront (Niles et al. 2009, p. 2). 
Peregrines are known to hunt shorebirds in the red knot's Virginia and 
Delaware Bay stopover areas (Niles 2010a; Niles et al. 2008, p. 106), 
and peregrine predation on red knots has been observed in Florida (A. 
Schwarzer pers. comm. June 17, 2013).
    Raptor predation has been shown to be an important mortality factor 
for shorebirds at several sites (Piersma et al. 1993, p. 349). However, 
Niles et al. (2008, p. 28) concluded that increased raptor populations 
have not been shown to affect the size of shorebird populations. Based 
on studies of other Calidris canutus subspecies in the Dutch Wadden 
Sea, Piersma et al. (1993, p. 349) concluded that the chance for an 
individual to be attacked and captured is small, as long as the birds 
remain in the open and in large flocks so that approaching raptors are 
likely to be detected. Although direct mortality from predation is 
generally considered relatively low in nonbreeding areas, predators 
also impact red knots by affecting habitat use and migration strategies 
(Niles et al. 2008, p. 101; Stillman et al. 2005, p. 215) and by 
causing disturbance, thereby potentially affecting red knots' rates of 
feeding and weight gain.
    Red knots' selection of high-tide roosting areas on the coast 
appears to be strongly influenced by raptor predation, something well 
demonstrated in other shorebirds (Niles et al. 2008, p. 28). Red knots 
require roosting habitats away from vegetation and structures that 
could harbor predators (Niles et al. 2008, p. 63). Red knots' usage of 
foraging habitat can also be affected by the presence of predators, 
possibly affecting the birds' ability to prepare for their final 
flights to the arctic breeding grounds (Watts 2009b) (e.g., if the 
knots are pushed out of those areas with the highest prey density or 
quality). In 2010, horseshoe crab egg densities were very high in 
Mispillion Harbor, Delaware, but red knot use was low because peregrine 
falcons were regularly hunting shorebirds in that area (Niles 2010a). 
Growing numbers of peregrine falcons on the Delaware Bay and New 
Jersey's Atlantic coasts are decreasing the suitability of a number of 
important shorebird areas (Niles 2010a). Analyzing survey data from the 
Virginia stopover area, Watts (2009b) found the density of red knots 
far (greater than 3.7 mi (6 km)) from peregrine nests was nearly eight 
times higher than close (0 to 1.9 mi (0 to 3 km)) to peregrine nests. 
In addition, red knot density in Virginia was significantly higher 
close to peregrine nests during those years when peregrine territories 
were not active compared to years when they were (Watts 2009b). Similar 
results were found for other Calidris canutus subspecies in the Dutch 
Wadden Sea, where the spatial distribution of C. canutus was best 
explained by both food availability and avoidance of predators (Piersma 
et al. 1993, p. 331).
    In addition to affecting habitat use, predation has been shown to 
affect migration strategies in Arctic-breeding shorebirds (Lank et al. 
2003, p. 303). Studying two other Calidris species, Hope et al. (2011, 
p. 522) found that both adults and juveniles shortened their stopover 
durations during the period of increased peregrine falcon abundance. 
Butler et al. (2003, p. 132) demonstrated how recovering raptor 
populations in North America appear to have led to changes in the 
migratory strategies of western sandpipers (C. mauri), including lower 
numbers of shorebirds, reduced stopover length, and lower body mass at 
the more predation-prone sites (as cited in Niles et al. 2008, p. 101).
    Red knots can also be affected by peregrines through repeated 
disturbance. Red knots in Virginia are frequently disturbed by 
peregrine falcons (Niles et al. 2008, p. 106). Peregrines flying near 
foraging shorebirds at Delaware Bay are known to cause severe 
disturbance, prompting the shorebirds to fly in evasive maneuvers and 
not return for prolonged time periods. It is not believed that 
disturbance by peregrines in Delaware Bay changed significantly over 
the time period that red knots declined (Breese 2010, pp. 3-4).
    The vulnerability of red knots, and their reactivity to perceived 
predation danger, may be related to their field of vision. Studying 
other subspecies, Martin and Piersma (2009, p. 437) found that Calidris 
canutus did not show comprehensive panoramic vision as found in some 
other tactile-feeding shorebirds, but have a binocular field 
surrounding the bill and a substantial blind area behind the head. This 
visual system may be a tradeoff for switching to more visually guided 
foraging (i.e., insects) on the breeding grounds. However, this 
forward-focused visual field leaves C. canutus vulnerable to aerial 
predation, especially when using tactile foraging in nonbreeding 
locations where predation by falcons is an important selection factor 
(Martin and Piersma 2009, p. 437).
    In the United States, most peregrine falcons in coastal areas rely 
on artificial nest sites (Niles et al. 2008, p. 101). In some areas, 
land managers have begun to remove peregrine nesting platforms in 
strategic locations where they are having the greatest impact on 
shorebirds (Niles 2010a; Watts 2009b; Kalasz 2008, p. 39).
    Peregrine falcon populations in the United States have increased 
substantially since the mid-1970s, when the bird was extirpated in the 
east and only 324 known nesting pairs remained in total (USFWS 2012b). 
Today there are from 2,000 to 3,000 breeding pairs of peregrine falcons 
in North America (USFWS 2012b). Other raptor populations also increased 
over this period due to stricter pesticide regulations and conservation 
efforts (Butler et al. 2003, p. 130). Such measures reduced the 
prevalence of DDT (dichloro-diphenyl-trichloroethane) in the 
environment, which had caused egg shell thinning and, therefore, poor 
nest productivity in peregrine falcons (USFWS 2012b). We expect that 
peregrine and other raptor populations will continue to grow over 
coming decades, but at a slower rate. We

[[Page 60057]]

also expect that land managers will continue balancing the conservation 
needs of both raptors and shorebirds, so that the predation pressures 
in key red knot wintering and stopover areas are likely to remain the 
same or decrease slightly.
    We conclude that, outside of the breeding grounds (which are 
discussed below), predation is not directly impacting red knot 
populations despite some direct mortality. At key stopover sites, 
however, localized predation pressures are likely to exacerbate other 
threats to red knot populations, such as habitat loss (Factor A), food 
shortages (Factor E), and asynchronies between the birds' stopover 
period and the occurrence of favorable food and weather conditions 
(Factor E). Predation pressures worsen these threats by pushing red 
knots out of otherwise suitable foraging and roosting habitats, causing 
disturbance, and possibly causing changes to stopover duration or other 
aspects of the migration strategy (see Cumulative Effects below).
Predation--Breeding Areas
    Although little information is available from the breeding grounds, 
the long-tailed jaeger (Stercorarius longicaudus) is prominently 
mentioned as a predator of red knot chicks in most accounts. Other 
avian predators include parasitic jaeger (S. parasiticus), pomarine 
jaeger (S. pomarinus), herring gull, glaucous gull (Larus hyperboreus), 
gyrfalcon (Falcon rusticolus), peregrine falcon, and snowy owl (Bubo 
scandiacus). Mammalian predators include arctic fox (Alopex lagopus) 
and sometimes arctic wolves (Canis lupus arctos) (Niles et al. 2008, p. 
28; COSEWIC 2007, p. 19). Predation pressure on Arctic-nesting 
shorebird clutches varies widely regionally, interannually, and even 
within each nesting season, with nest losses to predators ranging from 
close to 0 percent to near 100 percent (Meltofte et al. 2007, p. 20), 
depending on ecological factors.
    Abundance of arctic rodents, such as lemmings, is often cyclical, 
although less so in North America than in Eurasia. In the Arctic, 3- to 
4-year lemming cycles give rise to similar cycles in the predation of 
shorebird nests. When lemmings are abundant, predators concentrate on 
the lemmings, and shorebirds breed successfully. When lemmings are in 
short supply, predators switch to shorebird eggs and chicks (Niles et 
al. 2008, p. 101; COSEWIC 2007, p. 19; Meltofte et al. 2007, p. 21; 
USFWS 2003, p. 23; Blomqvist et al. 2002, p. 152; Summers and Underhill 
1987, p. 169). Blomqvist et al. (2002, p. 146) correlated predation 
pressure on Calidris canutus canutus on Siberian breeding grounds with 
numbers of juveniles in nonbreeding areas, following a 3-year cycle. 
These authors concluded that the reproductive output of C.c. canutus 
was limited by predation and that chick production was high when 
predation pressure was reduced by arctic foxes preying primarily on 
lemmings (Fraser et al. 2013, p. 13; Blomqvist et al. 2002, p. 146).
    In addition to affecting reproductive output, these cyclic 
predation pressures have been shown to influence shorebird nesting 
chronology and distribution. Studying 12 shorebird species, including 
red knot, over 11 years at 4 sites in the eastern Canadian Arctic, 
Smith et al. (2010a, pp. 292; 300) found that both snow conditions and 
predator abundance have significant effects on the chronology of 
breeding. Higher predator abundance resulted in earlier nesting than 
would be predicted by snow cover alone (Smith et al. 2010a, p. 292). 
Based on the adaptations of various species to deal with predators, 
Larson (1960, pp. 300-303) concluded that the distribution and 
abundance of Calidris canutus and other Arctic-breeding shorebirds were 
strongly influenced by arctic fox and rodent cycles, such that birds 
were in low numbers or absent in areas without lemmings because foxes 
preyed predominately on birds in those areas (as cited in Fraser et al. 
2013, p. 14).
    Years with few lemmings and many predators can be extremely 
unproductive for red knots, although predator cycles are usually not 
uniform across all breeding areas so that in most years there is 
generally some production of young (Niles et al. 2008, p. 63). 
Unsuccessful breeding seasons contributed to at least some of the 
observed reductions in the red knot population in the 2000s. However, 
rodent-predator cycles have always affected the productivity of Arctic-
breeding shorebirds and have generally caused only minor year-to-year 
changes in otherwise stable populations (Niles et al. 2008, pp. 64, 
    In northern Europe, lemming cycles diminished after the early 1990s 
but returned in the early 2000s (Fraser et al. 2013, p. 16; Brommer et 
al. 2010, p. 577; Kausrud et al. 2008, p. 93). Changes in temperature 
and humidity seemed to markedly affect rodent dynamics by altering 
conditions in the spaces below the snow where lemming prefer to live. 
These observations lead Kausrud et al. (2008, p. 93) to conclude that 
the pattern of less regular rodent peaks, and corresponding ecosystem 
changes mediated by predators, seem likely to prevail over a growing 
geographic area under projected climate change. However, Brommer et al. 
(2010, p. 577) found that lemming cycles in Finland returned after 
about 5 years despite ongoing and rapid climate change, suggesting that 
climate change may not explain why the cycles were interrupted.
    At two sites in northeast Greenland, lemming populations collapsed 
around 2000, both in terms of actual densities and periodicity (Schmidt 
et al. 2012, p. 4419). The observed change in Greenland lemming 
dynamics dramatically affected the predator guild, with the most 
pronounced response in two lemming-specialist predator species (Schmidt 
et al. 2012, p. 4421). Observed differences in predator responses 
between the two Greenland sites could arise from site-specific 
differences in lemming dynamics, interactions among predators, or 
subsidies from other resources (Schmidt et al. 2012, p. 4417) (e.g., 
shifting to other prey species, which could have implications for 
shorebirds). Ultimately, changing predator populations may cause 
cascading impacts on the entire tundra food web, with unknown 
consequences (Schmidt et al. 2012, p. 4421). Unlike the 1990s lemming 
cycle disruption in Europe, Schmidt et al. (2012, entire) did not 
report any signs of recovery of the Greenland lemming cycles, based on 
data through 2010.
    Disruption of rodent-predator cycles may constitute a large-scale 
impact on predation pressure on arctic shorebird nests (Meltofte et al. 
2007, p. 22). In the Siberian Arctic, lemmings are keystone species, 
and any climate effects on their abundance or population dynamics may 
indirectly affect shorebird populations through predation. The role of 
lemmings in the eastern Canadian Arctic is unclear, but large annual 
fluctuations in lemming or other rodent populations suggest that 
similar dynamics operate there (Meltofte et al. 2007, p. 34). Fraser et 
al. (2013, p. 13) investigated the relationship between the rodent 
cycle in Arctic Canada and numbers of red knots migrating through the 
United States. Shooting records from Cape Cod in the 1800s and red knot 
counts on Delaware Bay from 1986 to 1998 cycled with 4-year periods. 
Annual peaks in numbers of red knots stopping in the Delaware Bay from 
1986 to 1998 occurred 2 years after arctic rodent peaks, with a 
correlation more often than expected at random. These results suggest 
that red knot reproductive output was linked to the rodent cycle before 
the red knot population decline (i.e., 1998 and earlier). We have no 
evidence that such

[[Page 60058]]

a link existed after 1998. These findings are consistent with a 
hypothesis that an interruption of the rodent cycle in red knot 
breeding habitat could have been a driver in the red knot decline 
observed in the 2000s. However, additional studies would be needed to 
support this hypothesis (Fraser et al. 2013, p. 13).
    McKinnon et al. (2010, p. 326) used artificial nests to measure 
predation risk along a 2,083-mi (3,350-km) south-north gradient in the 
Canadian Arctic and found that nest predation risk declined more than 
twofold along the latitudinal gradient. The study area included the 
entire latitudinal range of known and modeled red knot breeding 
habitat, extending both farther south (into the sub-Arctic) and farther 
north (to encompass the breeding range of Calidris canutus islandica). 
Nest predation risk was negatively correlated with latitude. For an 
increase in 1[deg] of latitude, the relative risk of predation declined 
by 3.6 percent, equating to a 65 percent decrease in predation risk 
over the 29[deg] latitudinal transect. The results provide evidence 
that birds migrating farther north may acquire reproductive benefits in 
the form of lower nest predation risk (McKinnon et al. 2010, p. 326). 
Predation pressure on red knots could increase if, due to climate 
change, a new suite of predators expands their ranges northward from 
the sub-Arctic into the knot's breeding range.
    We conclude that cyclic predation in the Arctic results in years 
with extremely low reproductive output but does not threaten the red 
knot. The cyclical nature of this predation on shorebirds is a 
situation that has probably occurred over many centuries, and under 
historic conditions likely had no lasting impact on red knot 
populations. Where and when rodent-predator cycles are operating, we 
expect red knot reproductive success will also be cyclic. However, 
these cycles are being interrupted for reasons that are not yet fully 
clear. The geographic extent and duration of future interruptions to 
the cycles cannot be forecast but may intensify as the arctic climate 
changes. Disruptions in the rodent-predator cycle pose a substantial 
threat to red knot populations, as they may result in prolonged periods 
of very low reproductive output. Superimposed on these potential cycle 
disruptions are warming temperatures and changing vegetative conditions 
in the Arctic, which are likely to bring about additional changes in 
the predation pressures faced by red knots on the breeding grounds; we 
cannot forecast how such ecosystem changes are likely to unfold.
Factor C--Conservation Efforts
    We are unaware of any conservation efforts to reduce disease in red 
knots. We are also unaware of any conservation efforts to reduce 
predation of the red knot in its breeding range. As discussed above, 
land managers in some areas of the United States have begun to remove 
peregrine nesting platforms in key locations where they are having the 
greatest impact on shorebirds.
Factor C--Summary
    Red knots may be adapted to parasite-poor habitats and may, 
therefore, be susceptible to parasites when migrating or wintering in 
high-parasite regions. However, we have no evidence that parasites have 
affected red knot populations beyond causing normal, background levels 
of mortality, and we have no indications that parasite infection rates 
or red knot fitness impacts are likely to increase. Therefore, we 
conclude that parasites are not a threat to the red knot. For the most 
prevalent viruses found in shorebirds within the red knot's geographic 
range, infection rates in red knots are low, and health effects are 
minimal or have not been documented. Therefore, we conclude that viral 
infections do not cause significant mortality and are not a threat to 
the red knot. However, see Cumulative Effects (below) regarding an 
unlikely but potentially high-impact, synergistic effect among avian 
influenza, environmental contaminants, and climate change in Delaware 
    Outside of the breeding grounds, predation is not affecting red 
knot populations despite some direct mortality. At key stopover sites, 
however, localized predation pressures are likely to exacerbate other 
threats to red knot populations by pushing red knots out of otherwise 
suitable foraging and roosting habitats, causing disturbance, and 
possibly causing changes to stopover duration or other aspects of the 
migration strategy. We expect the direct and indirect effects of 
predators to continue at the same level or decrease slightly over the 
next few decades.
    Within the breeding range, normal 3- to 4-year cycles of high 
predation, mediated by rodent cycles, result in years with extremely 
low reproductive output but do not threaten the survival of the red 
knot at the subspecies level. However, these rodent-predator cycles are 
being interrupted for reasons that are not yet fully clear but may be 
linked to climate change. Disruptions in the rodent-predator cycle pose 
a substantial threat to the red knot, as they may result in prolonged 
periods of very low reproductive output. Such disruptions have already 
occurred and may increase due to climate change. The substantial 
impacts of elevated egg and chick predation on shorebird reproduction 
are well known, although the red knot's capacity to adapt to long-term 
changes in predation pressure is unknown. The threat of persistent 
increases in predation in the Arctic may already be having subspecies-
level effects and is anticipated to increase into the future. Further, 
warming temperatures and changing vegetative conditions in the Arctic 
are likely to bring additional changes in the predation pressures faced 
by red knots, but we cannot forecast how such ecosystem changes are 
likely to unfold.
Factor D. The Inadequacy of Existing Regulatory Mechanisms
    Under this factor, we examine the effects of existing regulatory 
mechanisms in relation to the threats to the red knot discussed under 
the other four factors. Section 4(b)(1)(A) of the Act requires the 
Service to take into account ``those efforts, if any, being made by any 
State or foreign nation, or any political subdivision of a State or 
foreign nation, to protect such species . . .'' In relation to Factor D 
under the Act, we interpret this language to require the Service to 
consider relevant Federal, state, and tribal laws, regulations, and 
other such mechanisms that may reduce any of the threats we describe in 
our threat analyses under the other four factors. We give strongest 
weight to statutes and their implementing regulations and to management 
direction that stems from those laws and regulations. An example would 
be State governmental actions enforced under a State statute, or 
Federal actions under Federal statute.
    A comprehensive discussion of international, Federal, State, and 
local laws, regulations, policies, and treaties that apply to the red 
knot is available as a supplemental document (``Factor D: The 
Inadequacy of Existing Regulatory Mechanisms'') on the Internet at 
http://www.regulations.gov (Docket No. FWS-R5-ES-2013-0097; see 
ADDRESSES section for further access instructions). We provide a brief 
summary below.
    In Canada, the Species at Risk Act provides protections for the red 
knot and its habitat, both on and off Federal lands. The red knot is 
afforded additional protections under the Migratory Birds Convention 
Act and by provincial law in four of Canada's Provinces. In other areas 
outside of the United States' jurisdiction, red knots are legally 
protected from direct take and hunting in several Caribbean and Latin

[[Page 60059]]

American countries, but we lack information regarding the 
implementation or effectiveness of these measures (see Factor B--
Hunting). For many other countries, red knot hunting is unregulated, or 
we lack sufficient information to determine if red knot hunting is 
legal. We also lack information for countries outside the United States 
regarding the protection or management of red knot habitat, and 
regarding the regulation of other activities that threaten the red knot 
such as development (see Factor A--International Coastal Development) 
and disturbance, oil spills, environmental contaminants, and wind 
energy development (see Factor E).
    Within the United States, the Migratory Bird Treaty Act of 1918 (16 
U.S.C. 703 et seq.) (MBTA) and state wildlife laws protect the red knot 
from direct take resulting from scientific study and hunting (see 
Factor B). The MBTA is the only Federal law in the United States 
currently providing specific protection for the red knot due to its 
status as a migratory bird. The MBTA prohibits the following actions, 
unless permitted by Federal regulation: To ``pursue, hunt, take, 
capture, kill, attempt to take, capture or kill, possess, offer for 
sale, sell, offer to purchase, purchase, deliver for shipment, ship, 
cause to be shipped, deliver for transportation, transport, cause to be 
transported, carry, or cause to be carried by any means whatever, 
receive for shipment, transportation or carriage, or export, at any 
time, or in any manner, any migratory bird . . . or any part, nest, or 
egg of any such bird.'' Through issuance of Migratory Bird Scientific 
Collecting permits, the Service ensures that best practices are 
implemented for the careful capture and handling of red knots during 
banding operations and other research activities (see Factor B--
Scientific Study). Birds in the Family Scolopacidae, including the red 
knot, are listed as a game species under international treaties with 
Canada and Mexico. The MBTA, which implements these treaties, grants 
the Service authority to establish hunting seasons for any listed game 
species. However, the Service has determined that hunting is 
appropriate only for those species for which there is a long tradition 
of hunting, and for which hunting is consistent with their population 
status and their long-term conservation. The Service would not consider 
legalizing the hunting of shorebird species, such as the red knot, 
whose populations were previously devastated by market hunting (USFWS 
2012c) (see Factor B--Hunting).
    There are no provisions in the MBTA that prevent habitat 
destruction unless the activity causes direct mortality or the 
destruction of active nests, which would not apply since red knots do 
not breed in the United States. The MBTA does not address threats to 
the red knot from further population declines associated with habitat 
loss, insufficient food resources, climate change, or the other threats 
discussed under Factors A, B, C, and E. However, the Sikes Act (16 
U.S.C. 670), covering military bases, the National Park Service Organic 
Act of 1916, as amended (NPSOA), covering national parks and seashores, 
and the National Wildlife Refuge System Improvement Act of 1997 
(NWRSIA), covering national wildlife refuges, do provide protection for 
the red knot from habitat loss and inappropriate management on Federal 
    Among coastal States from Maine to Texas, all except Alabama have 
enacted some kind of endangered species legislation; however, the red 
knot is listed only in New Jersey (as endangered) and Georgia (as rare, 
a category of protected species). The New Jersey Endangered and Non 
Game Species Conservation Act of 1973 (N.J.S.A. 23:2A et seq.) 
prohibits taking, possessing, transporting, exporting, processing, 
selling, or shipping listed species. ``Take'' is defined in New Jersey 
as harassing, hunting, capturing, or killing, or attempting to do so. 
As a State-listed species, the red knot is also afforded habitat 
protection under the New Jersey Coastal Zone Rules (N.J.A.C. 7:7E). 
Under the Georgia Nongame and Endangered Species Conservation Act (Code 
1976 Sec.  50-15-10-90), red knots cannot be captured, killed, or sold, 
and their habitat is protected on public lands; however, Georgia law 
specifically states that rules and regulations related to the 
protection of State-protected species shall not affect rights in 
private property.
    As discussed under Factors A and E, shoreline stabilization has 
significant impacts on red knot habitats, and can also impact knots 
through disturbance and via impacts on prey resources. Shoreline 
stabilization is often federally funded (e.g., through the Water 
Resources Development Acts) or authorized (e.g., under section 404 of 
the Clean Water Act (33 U.S.C. 1251 et seq.) and sections 9 and 10 of 
the Rivers and Harbors Act (33 U.S.C. 403 et seq.)). Federal funding or 
authorization for a project triggers several environmental requirements 
that may afford some protections to red knots or their habitats, but 
several of these are nonregulatory in nature (e.g., the National 
Environmental Policy Act 42 U.S.C. 4321 et seq. (1969) (NEPA); 
Executive Order 13186 (Responsibilities of Federal Agencies to Protect 
Migratory Birds)). One regulatory measure is the Coastal Barrier 
Resources Act (Pub. L. 97-348) (96 Stat. 1653; 16 U.S.C. 3501 et seq.) 
(CBRA), as amended. The CBRA designated relatively undeveloped coastal 
barriers along the Atlantic and Gulf coasts as part of the John H. 
Chafee Coastal Barrier Resources System and made these areas ineligible 
for most new Federal expenditures and financial assistance, including 
Federal flood insurance that can promote development. The goal of these 
laws is to remove Federal incentives for the development of coastal 
barriers (e.g., barrier islands), because such development can lead to 
loss of natural resources, threats to human life and property, and 
imprudent expenditure of tax dollars.
    The Coastal Zone Management Act of 1972 (Pub. L. 92-583) (86 Stat. 
1280; 16 U.S.C. 1451-1464) (CZMA) provides Federal funding to implement 
the States' federally approved Coastal Zone Management Plans, which 
guide and regulate development and other activities within the 
designated coastal zone of each State. All eligible States in the red 
knot's U.S. range (including the Great Lakes) have approved Coastal 
Zone Management Plans (National Oceanic and Atmospheric Administration 
(NOAA) 2012c, p. 2). In those States with approved plans, the CZMA 
requires Federal action agencies to ensure that the activities they 
fund or authorize are consistent, to the maximum extent practicable, 
with the enforceable policies of that State's federally approved 
coastal management program; this provision of CZMA is known as Federal 
consistency (NOAA 2012c, p. 2). Thirteen of 18 Atlantic or Gulf coast 
States (72 percent) range allow for new hard structures along the 
oceanfront beach, and 16 of these 18 States allow armoring of bays and 
sounds (Rice 2012a, p. 7; Titus 2000, p. 743). As of 2000, every State 
from Maine to Texas allowed oceanfront beach nourishment, although 
beach nourishment of bays and sounds was permitted in only 7 of these 
18 States (Titus 2000, p. 743). Due to the CZMA's Federal consistency 
provision, Federal agencies also generally follow each State's policies 
in determining if coastal projects may be federally funded or 
    Other threats to habitat and food supplies and from disturbance are 
partially, but not fully, abated by various State and Federal 
regulations. First, State regulations provide varying levels of 
protection from impacts

[[Page 60060]]

associated with beach grooming (i.e., mechanical raking or cleaning), 
but we do not have comprehensive information for each State. Above the 
high tide line, beach grooming activities are typically not regulated 
by the USACE, and thus fall under State and local jurisdictions. In 
those jurisdictions for which information is available, beach grooming 
is generally permitted in red knot habitat, including while the birds 
are present. Second, several Federal and State regulatory and 
nonregulatory measures are in effect to stem the introductions and 
effects of invasive and harmful species (e.g., Executive Order 13112; 
the Plant Protection Act of 2000 (Pub. L. 106-224); the Nonindigenous 
Aquatic Nuisance Prevention and Control Act of 1990 (Pub. L. 101-646); 
the National Invasive Species Act of 1996 (Pub. L. 104-332); the U.S. 
Coast Guard's (USCG) ballast water regulations (77 FR 17254); the Lacey 
Act (18 U.S.C. 42, 50 CFR part 16); the Clean Water Act; and the 
Harmful Algal Bloom and Hypoxia Amendments Act of 2004 (Pub. L. 108-
456)), but collectively these measures do not provide complete 
protection to the red knot from impacts to its habitats or food 
supplies resulting from beach or marine invaders or the spread of 
harmful algal species. Third, although threats to the horseshoe crab 
egg resource remain (see Factor E--Reduced Food Supplies), the current 
regulatory management of the horseshoe crab fishery (e.g., the Adaptive 
Resource Management (ARM) framework adopted by the ASMFC, a governing 
body established by the Atlantic Coastal Fisheries Cooperative 
Management Act of 1993) is adequately addressing threats to the knot's 
Delaware Bay food supply from direct harvest of horseshoe crabs. 
Fourth, although we lack information regarding the overall effect of 
recreation management policies on the red knot, we are aware of a few 
locations in which beaches are closed, regulated, or monitored to 
protect nonbreeding shorebirds through the MBTA, Sikes Act, NPSOA, 
NWRSIA, and State or local laws and policies. And fifth, relatively 
strong Federal laws likely reduce risks to red knots from oil spills 
(e.g., the Oil Pollution Act of 1990 (OPA) (33 U.S.C. 2701 et seq.)) 
and pesticides (e.g., the Federal Insecticide, Fungicide, and 
Rodenticide Act (7 U.S.C. 136 et seq.)). The OPA requires contingency 
planning by Federal, state, and local governments and industry groups, 
and includes penalties for regulatory noncompliance. Under the OPA, the 
EPA regulates above ground storage facilities and the USCG regulates 
oil tankers, which have been transitioning to double hulls since 1992 
under international agreements. In addition, oil and gas operations on 
the Outer Continental Shelf (OCS) are regulated (50 CFR parts 203-291) 
by the Bureau of Safety and Environmental Enforcement (BSEE) within the 
Department of the Interior (DOI). Despite the relatively robust oil 
spill and pesticide regulations in place, these laws have not been 
sufficient to prevent documented shorebird mortalities and other 
impacts in recent decades.
    In addition to above-mentioned regulatory mechanisms addressing 
threats to habitat, food resources, and from disturbance, there are 
Federal laws and policies to reduce the red knot's collision risks from 
new terrestrial and offshore wind turbine development (e.g., 
construction and operation). The MBTA applies to all Federal and non-
Federal activities that result in the ``take'' of migratory birds. To 
assist wind developers comply with MBTA, the Service's voluntary Land-
Based Wind Energy Guidelines provide a structured, scientific process 
for addressing wildlife conservation concerns at all stages of land-
based wind energy development (USFWS 2012d, p. vi). In addition to the 
MBTA, other Federal regulatory mechanisms and nonregulatory policies 
(e.g., NEPA, Executive Order 13186, NSPOA, NWRSIA, and section 10 of 
the Endangered Species Act) may apply to terrestrial wind energy 
development, depending on the nature of the Federal nexus, if any, in 
turbine construction and operation. Regarding offshore wind energy 
development, section 388 of the Energy Policy Act of 2005 granted the 
DOI discretionary authority to issue leases, easements, or rights-of-
way for activities on the OSC for wind and other types of renewable 
energy development. Under NEPA, DOI has prepared a Programmatic 
Environmental Impact Statement setting forth policies and best 
management practices, and has promulgated regulations and guidelines 
(Department of Energy (DOE) and Bureau of Ocean Energy Management, 
Regulation, and Enforcement (BOEMRE) 2011, p. iii). In addition to 
these Federal provisions, some states have policies in place to address 
risks to red knots from wind energy development (see supplemental 
document--Factor D). However, as described below in Factor E, despite 
these state and Federal laws, policies, and voluntary guidelines, we 
expect some level of red knot mortality to occur from the buildout of 
the Nation's wind energy infrastructure.
Factor E. Other Natural or Manmade Factors Affecting Its Continued 
    In this section, we present and assess the best available 
information regarding a range of other ongoing and emerging threats to 
the red knot, including reduced food availability, asynchronies 
(``mismatches'') between the timing of the red knot's annual cycle and 
the windows of optimal food and weather conditions on which it depends, 
human disturbance, oil spills, environmental contaminants, and wind 
energy development.
Factor E--Reduced Food Availability
    Declining food resources can have major implications for the 
survival and reproduction of long-distance migrant shorebirds 
(International Wader Study Group 2003, p. 10). The life history of 
long-distance, long-hop migrant shorebirds indicates that the 
availability of abundant food resources at temperate stopovers is 
critical for completing their annual cycle (USFWS 2003, p. 4). In other 
Calidris canutus subspecies, commercial shellfish harvests have been 
linked to local decreases in recruitment and possibly emigration in a 
wintering area in England (Atkinson et al. 2003a, p. 127); increased 
gizzard sizes (possibly to grind lower quality, i.e., thicker shelled, 
prey) and decreases in local survival in a wintering area in the Dutch 
Wadden Sea (van Gils et al. 2006, p. 2399); and prey switching and 
reduced red knot use in a wintering and stopover area in the Dutch 
Wadden Sea (Piersma et al. 1993, pp. 343, 354). Harvest activities have 
also been shown to impact prey availability for other Calidris 
species--foraging efficiency of semipalmated sandpipers decreased 
nearly 70 percent after 1 year of baitworm harvesting in the Bay of 
Fundy, concurrent with habitat changes and a 39 percent decrease in the 
sandpiper's preferred amphipod prey (Shepherd and Boates 1999, p. 347).
    Commercial harvest of horseshoe crabs has been implicated as a 
causal factor in the decline of the rufa red knot, by decreasing the 
availability of horseshoe crab eggs in the Delaware Bay stopover (Niles 
et al. 2008, pp. 1-2). Notwithstanding the importance of the horseshoe 
crab and Delaware Bay, other lines of evidence suggest that the rufa 
red knot also faces threats to its food resources throughout its range. 
The following discussion addresses known or likely threats to the 
abundance or quality of red knot prey. Potential food shortages caused 
by asynchronies (``mismatches'') in the red knot's annual cycle are 
discussed in the next section.

[[Page 60061]]

Also see Factor A--Agriculture and Aquaculture, above, regarding clam 
farming practices in Canada that impact red knot prey resources by 
modifying suitable foraging habitat via sediment sifting. Although 
threats to food quality and quantity are widespread, red knots in 
localized areas have shown some ability to switch prey when the 
preferred prey species became reduced (Escudero et al. 2012, pp. 359, 
362; Musmeci et al. 2011, entire), suggesting some adaptive capacity to 
cope with this threat.
Food Availability--Ocean Acidification
    During most of the year, bivalves and other mollusks are the 
primary prey for the red knot (see the ``Migration and Wintering Food'' 
section of the Rufa Red Knot Ecology and Abundance supplemental 
document). Mollusks in general are at risk from climate change-induced 
ocean acidification (Fabry et al. 2008, pp. 419-420). Oceans become 
more acidic as carbon dioxide emitted into the atmosphere dissolves in 
the ocean. The pH (percent hydrogen, a measure of acidity or 
alkalinity) level of the oceans has decreased by approximately 0.1 pH 
units since preindustrial times, which is equivalent to a 25 percent 
increase in acidity. By 2100, the pH level of the oceans is projected 
to decrease by an additional 0.3 to 0.4 units under the highest 
emissions scenarios (NRC 2010, pp. 285-286). As ocean acidification 
increases, the availability of calcium carbonate declines. Calcium 
carbonate is a key building block for the shells of many marine 
organisms, including bivalves and other mollusks (USEPA 2012; NRC 2010, 
p. 286). Vulnerability to ocean acidification has been shown in bivalve 
species similar to those favored by red knots, including mussels 
(Gaylord et al. 2011, p. 2586; Bibby et al. 2008, p. 67) and clams 
(Green et al. 2009, p. 1037). Reduced calcification rates and calcium 
metabolism are also expected to affect several mollusks and crustaceans 
that inhabit sandy beaches (Defeo et al. 2009, p. 8), the primary 
nonbreeding habitat for red knots. Relevant to Tierra del Fuego-
wintering knots, bivalves have also shown vulnerability to ocean 
acidification in Antarctic waters, which are predicted to be 
particularly affected due to naturally low carbonate saturation levels 
in cold waters (Cummings et al. 2011, p. 1).
    To study the effects of ocean acidification on marine 
invertebrates, Hale et al. (2011, p. 661) collected representative 
species, including mollusks, from the extreme low intertidal zone and 
exposed them in the laboratory to varying levels of pH and temperature. 
These authors found significant changes in community structure and 
lower diversity in response to reduced pH. At lower pH levels, warmer 
temperatures resulted in lower species abundances and diversity. The 
species losses responsible for these changes in community structure and 
diversity were not randomly distributed across the different phyla 
examined, with mollusks showing the greatest reduction in abundance and 
diversity in response to low pH and elevated temperature. This and 
other studies support the idea that ocean acidification-induced changes 
in marine biodiversity will be driven by differential vulnerability 
within and between different taxonomic groups. This study also 
illustrates the importance of considering indirect effects that occur 
within multispecies assemblages when attempting to predict the 
consequences of ocean acidification and global warming on marine 
communities (Hale et al. 2011, p. 661). With climate change, 
interactions between temperature and pH may cause detrimental 
ecological changes to red knot prey species at both wintering and 
migration stopover areas.
Food Availability--Temperature Changes
    In addition to being sensitive to acidification, mollusks and other 
marine invertebrates are sensitive to temperature changes. Global 
average air temperature is expected to warm at least twice as much in 
the next century as it has over the previous century, with an expected 
increase of 2 to 11.5 [deg]F (1.1 to 6.4 [deg]C) by 2100 (USEPA 2012). 
Coastal waters are ``very likely'' to continue to warm by as much as 4 
to 8 [deg]F (2.2 to 4.4 [deg]C) in this century, both in summer and 
winter (USGCRP 2009, p. 151). In the mid-Atlantic, changes in water 
temperature (and quality) are expected to have mostly indirect effects 
on red knots and other shorebirds, primarily through changes in the 
distribution and abundance of food resources (Najjar et al. 2000, p. 
227). Changes in sea temperatures can have major effects on marine 
populations, as witnessed during severe events such as El Ni[ntilde]o 
(an occasional abnormal warming of tropical waters in the eastern 
Pacific from unknown causes), when the abundance of many invertebrate 
species plummeted on South American beaches (Rehfisch and Crick 2003, 
p. 88). Although the invertebrates recovered quickly when conditions 
returned to normal, this short-term change in sea temperature may give 
an indication of likely changes under projected global warming 
scenarios (Rehfisch and Crick 2003, p. 88).
    Asynchronies (``mismatches'') between the timing of the red knot's 
annual cycle and the peak abundance periods of its prey are discussed 
in the next section. However, repeated asynchronies can also occur 
between a prey species' own annual cycles and environmental conditions, 
leading to long-term declines of these invertebrate populations and 
thereby affecting the absolute quantity of red knot food supplies (in 
addition to the timing). For example, Philippart et al. (2003, p. 2171) 
found that rising water temperatures upset the timing of reproduction 
in the intertidal bivalve Macoma balthica, with the timing of the first 
vulnerable life stages thrown out of sync with respect to the most 
optimal environmental conditions (a phytoplankton bloom and the 
settlement of juvenile shrimps). These authors concluded that prolonged 
periods of lowered bivalve recruitment and stocks may lead to a 
reformulation of estuarine food webs and possibly a reduction of the 
resilience of the system to additional disturbances, such as shellfish 
harvest (Philippart et al. 2003, p. 2171).
    Blue mussel spat is an important prey item for red knots in 
Virginia (Karpanty et al. 2012, p. 1). The southern limit of adult blue 
mussels has contracted from North Carolina to Delaware since 1960 due 
to increasing air and water temperatures (Jones et al. 2010, pp. 2255-
2256). Larvae have continued to recruit to southern locales (including 
Virginia) via currents, but those recruits die early in the summer due 
to water and air temperatures in excess of lethal physiological limits. 
Failure to recolonize southern regions will occur when reproducing 
populations at higher latitudes are beyond dispersal distance (Jones et 
al. 2010, pp. 2255-2256). Thus, this key prey resource may soon 
disappear from the red knot's Virginia spring stopover habitats 
(Karpanty et al. 2012, p. 1).
Food Availability--Other Aspects of Climate Change
    Invertebrate prey species may also be affected by other aspects of 
climate change. For example, freshwater inputs, tidal prisms (the 
volume of water in an estuary between high and low tide), and salinity 
regimes may be much altered, which could significantly alter the 
composition of estuarine communities. Furthermore, rising sea levels 
are expected to affect the physical shape (e.g., dimensions, 
configuration) of estuaries, changing their sediment compositions. This 
habitat change in

[[Page 60062]]

turn would change invertebrate densities and community composition, 
thus affecting shorebirds (Rehfisch and Crick 2003, p. 88; Najjar et 
al. 2000, p. 225), such as the red knot.
Food Availability--Disease, Parasites, Invasive Species, and Unknown 
    Red knot prey species are also vulnerable to disease, parasites, 
invasive species, and unknown factors influencing their quality and 
quantity. For example, at the single largest wintering area, 
Bah[iacute]a Lomas on Tierra del Fuego in Chile, Espoz et al. (2008, 
pp. 69, 74) found that most (91 percent) of the prey (the clam Darina 
solenoides) were much smaller and, therefore, probably less 
energetically profitable than the size classes of bivalves shown to be 
preferred by knots in many other locations. These authors suggest that 
food supply at Bah[iacute]a Lomas may be a limiting factor for the knot 
population and might have contributed to population declines in the 
2000s. However, no reasons for the small prey size are known (Espoz et 
al. 2008, p. 75), and it is unknown whether prey size in this area has 
decreased over time.
    In R[iacute]o Grande, Argentina, a key Tierra del Fuego wintering 
area, Escudero et al. (2012) sampled the area's two main red knot prey 
types (Mytilidae mussels and the clam Darina solenoides) in 1995, 2000, 
and 2008. Over the study period, significant decreases occurred in the 
sizes of available prey items and in the red knots' energy intake 
rates. Intake rates went from the highest known for red knots anywhere 
in the world in 2000 to among the lowest in 2008 (Escudero et al. 2012, 
pp. 359-362). These authors also found a substantial increase in the 
rate of red knots utilizing alternate prey species, and their findings 
imply that the birds incorporated other prey types into their diets to 
increase intake rates (Escudero et al. 2012, pp. 359, 362). No 
explanation is available for the decline in prey sizes. Escudero et al. 
(2012, p. 363) noted a high prevalence of a digenean parasite 
(Bartolius pierrei) on D. solenoides clams. These authors do not 
implicate the parasite in the declining sizes of available clams. The 
mussels, which were not subject to any noteworthy parasitism, also 
exhibited decreased sizes over the study period (Escudero et al. 2012, 
p. 359), suggesting that parasitism is not a likely explanation for 
declining sizes. However, disease and parasites of the red knots' 
mollusk prey may increase with climate change, with potential effects 
on both prey availability and the health of the birds exposed to these 
pathogens. Increases in mollusk diseases, apparently temperature-
related, were detected in a review of scientific literature published 
from 1970 to 2001 (Ward and Lafferty 2004, p. 543).
    Globally, coastal marine habitats are among the most heavily 
invaded systems, stemming in part from human-mediated transport of 
nonnative species in the ballast of ships and from intentional 
introductions for aquaculture and fisheries enhancement (Grosholz 2002, 
p. 22). For example, introduction of nonnative oysters (Crassostrea 
spp.) has been widespread within the range of the red knot (Ruesink et 
al. 2005, p. C-1). Worldwide, introduced oysters have been vectors for 
several invasive species of marine algae, invertebrates, and protozoa 
(Ruesink et al. 2005, pp. 669-670). Invasive species can cause disease 
in native mollusks, displace native invertebrates through competition 
or predation, alter ecosystems, and affect species at higher trophic 
levels such as shorebirds (Ruesink et al. 2005, pp. 671-674; Grosholz 
2002, p. 23).
Food Availability--Sediment Placement
    The quantity and quality of red knot prey may also be affected by 
the placement of sediment for beach nourishment or disposal of dredged 
material (see Factor A above for a discussion of the extent of these 
practices in the United States and their effects on red knot habitat). 
Invertebrates may be crushed or buried during project construction. 
Although some benthic species can burrow through a thin layer of 
additional sediment, thicker layers (over 35 in (90 cm)) smother the 
benthic fauna (Greene 2002, p. 24). By means of this vertical 
burrowing, recolonization from adjacent areas, or both, the benthic 
faunal communities typically recover. Recovery can take as little as 2 
weeks or as long as 2 years, but usually averages 2 to 7 months (Greene 
2002, p. 25; Peterson and Manning 2001, p. 1). Although many studies 
have concluded that invertebrate communities recovered following sand 
placement, study methods have often been insufficient to detect even 
large changes (e.g., in abundance or species composition), due to high 
natural variability and small sample sizes (Peterson and Bishop 2005, 
p. 893). Therefore, uncertainty remains about the effects of sand 
placement on invertebrate communities, and how these impacts may affect 
red knots.
    The invertebrate community structure and size class distribution 
following sediment placement may differ considerably from the original 
community (Zajac and Whitlatch 2003, p. 101; Peterson and Manning 2001, 
p. 1; Hurme and Pullen 1988, p. 127). Recovery may be slow or 
incomplete if placed sediments are a poor grain size match to the 
native beach substrate (Bricker 2012, pp. 31-33; Peterson et al. 2006, 
p. 219; Greene 2002, pp. 23-25; Peterson et al. 2000, p. 368; Hurme and 
Pullen 1988, p. 129), or if placement occurs during a seasonal low 
point in invertebrate abundance (Burlas 2001, p. 2-20). Recovery is 
also affected by the beach position and thickness of the deposited 
material (Schlacher et al. 2012, p. 411). If the profile of the 
nourished beach and the imported sediments do not match the original 
conditions, recovery of the benthos is unlikely (Defeo et al. 2009, p. 
4). Reduced prey quantity and accessibility caused by a poor sediment 
size match have been shown to affect shorebirds, causing temporary but 
large (70 to 90 percent) declines in local shorebird abundance 
(Peterson et al. 2006, pp. 205, 219).
    Beach nourishment is a regular practice on the Delaware side of 
Delaware Bay and can affect spawning habitat for horseshoe crabs. 
Although beach nourishment generally preserves habitat value better 
than hard stabilization structures, nourishment can enhance, maintain, 
or decrease habitat value depending on beach geometry and sediment 
matrix (Smith et al. 2002a, p. 5). In a field study in 2001 and 2002, 
Smith et al. (2002a, p. 45) found a stable or increasing amount of 
spawning activity at beaches that were recently nourished while 
spawning activity at control beaches declined. These authors also found 
that beach characteristics affect horseshoe crab egg development and 
viability. Avissar (2006, p. 427) modeled nourished versus control 
beaches and found that nourishment may compromise egg development and 
viability. Despite possible drawbacks, beach nourishment has been 
recommended to prevent the loss of spawning habitat for horseshoe crabs 
(Kalasz 2008, p. 34; Carter et al. in Guilfoyle et al. 2007, p. 71; 
ASMFC 1998, p. 28) and is being pursued as a means of restoring 
shorebird habitat in Delaware Bay following Hurricane Sandy (Niles et 
al. 2013, entire; USACE 2012, entire). In areas of Delaware Bay with 
hard stabilization structures or high erosion rates, beach nourishment 
may be the only option for maintaining habitat.
Food Availability--Recreational Activities
    Recreational activities can likewise affect the availability of 
shorebird food resources by causing direct mortality of

[[Page 60063]]

prey. Studies from the United States and other parts of the world have 
documented recreational impacts to beach invertebrates, primarily from 
the use of off-road vehicles (ORVs), but even heavy pedestrian traffic 
can have effects. Few studies have examined the potential link between 
these invertebrate impacts and shorebirds. However, several studies on 
the effects of recreation on invertebrates are considered the best 
available information, as they involve species and habitats similar to 
those used by red knots.
    Although pedestrians exert relatively low ground pressures, 
extremely heavy foot traffic can cause direct crushing of intertidal 
invertebrates. In South Africa, Moffett et al. (1998, p. 87) found the 
clam Donax serra was slightly affected at all trampling intensities, 
while D. sordidus and the isopod Eurydice longicornis were affected 
only at high trampling intensities. Few members of the macrofauna were 
damaged at low trampling intensities, but substantial damage occurred 
under intense trampling (Moffett et al. 1998, p. 87). At beach access 
points in Australia, Schlacher and Thompson (2012, pp. 123-124) found 
trampling impacts to benthic invertebrates on the lower part of the 
beach, including significant reductions in total abundance and species 
richness and a shift in community structure. Studies have found that 
macrobenthic populations and communities respond negatively to 
increased human activity, but not in all cases. In addition, it can be 
difficult to separate the effect of human trampling from habitat 
modifications because these often coincide in high-use areas. In 
general, evidence is sparse about how sensitive intertidal 
invertebrates might be to human trampling (Defeo et al. 2009, p. 3). We 
are not aware of any studies looking at potential links between 
trampling and shorebird prey availability, but red knots often occur in 
areas with high recreational use (see Human Disturbance, below).
    In many areas, habitat for the piping plover overlaps considerably 
with red knot habitats. A preliminary review of ORV use at piping 
plover wintering locations (from North Carolina to Texas) suggests that 
ORV impacts may be most widespread in North Carolina and Texas (USFWS 
2009, p. 46). Although red knots normally feed low on the beach, they 
may also utilize the wrack line (see the ``Migration and Wintering 
Habitat'' section of the Rufa Red Knot Ecology and Abundance 
supplemental document, and Factor A--Beach Cleaning). Kluft and 
Ginsberg (2009, p. vi) found that ORVs killed and displaced 
invertebrates and lowered the total amount of wrack, in turn lowering 
the overall abundance of wrack dwellers. In the intertidal zone, 
invertebrate abundance is greatest in the top 12 in (30 cm) of sediment 
(Carley et al. 2010, p. 9). Intertidal fauna are burrowing organisms, 
typically 2 to 4 in (5 to 10 cm) deep; burrowing may ameliorate direct 
crushing. However, shear stress of ORVs can penetrate up to 12 in (30 
cm) into the sand (Schlacher and Thompson 2007, p. 580).
    Some early studies found minimal impacts to intertidal beach 
invertebrates from ORV use (Steinback and Ginsberg 2009, pp. 4-6; Van 
der Merwe and Van der Merwe 1991, p. 211; Wolcott and Wolcott 1984, p. 
225). However, some attempts to determine whether ORVs had an impact on 
intertidal fauna have been unsuccessful because the naturally high 
variability of these invertebrate communities masked any effects of 
vehicle damage (Stephenson 1999, p. 16). Based on a review of the 
literature through 1999, Stephenson (1999, p. 33) concluded that 
vehicle impacts on the biota of the foreshore (intertidal zone) of 
sandy beaches have appeared to be minimal, at least when the vehicle 
use occurred during the day when studies typically take place, but very 
few elements of the foreshore biota had been examined.
    Other studies have found higher impacts to benthic invertebrates 
from driving (Sheppard et al. 2009, p. 113; Schlacher et al. 2008b, pp. 
345, 348; Schlacher et al. 2008c, pp. 878, 882; Wheeler 1979, p. iii), 
although it can be difficult to discern results specific to the wet 
sand zone where red knots typically forage. Due to the compactness of 
sediments low on the beach profile, driving in this zone is thought to 
minimize impacts to the invertebrate community. However, the relative 
vulnerability of species in this zone is not well known, and driving 
low on the beach may expose a larger proportion of the total intertidal 
fauna to vehicles (Schlacher and Thompson 2007, p. 581). The severity 
of direct impacts (e.g., crushing) depends on the compactness of the 
sand, the sensitivity of individual species, and the depth at which 
they are buried in the sand (Schlacher et al. 2008b, p. 348; Schlacher 
et al. 2008c, p. 886). At least one study documented a positive 
response of shorebird populations following the exclusion of ORVs 
(Defeo et al. 2009, p. 3; Williams et al. 2004, p. 79), although the 
response could have been due to decreased disturbance (discussed below) 
as well as (or instead of) increased prey availability following the 
    In summary, several studies have shown impacts from recreational 
activities on invertebrate species typical of those used by red knots, 
and in similar habitats. The extent to which mortality of beach 
invertebrates from recreational activities propagates through food webs 
is unresolved (Defeo et al. 2009, p. 3). However, we conclude that 
these activities likely cause at least localized reductions in red knot 
prey availability.
Food Availability--Horseshoe Crab Harvest
    Reduced food availability at the Delaware Bay stopover site due to 
commercial harvest and subsequent population decline of the horseshoe 
crab is considered a primary causal factor in the decline of the rufa 
subspecies in the 2000s (Escudero et al. 2012, p. 362; McGowan et al. 
2011a, pp. 12-14; CAFF 2010, p. 3; Niles et al. 2008, pp. 1-2; COSEWIC 
2007, p. vi; Gonz[aacute]lez et al. 2006, p. 114; Baker et al. 2004, p. 
875; Morrison et al. 2004, p. 67), although other possible causes or 
contributing factors have been postulated (Fraser et al. 2013, p. 13; 
Schwarzer et al. 2012, pp. 725, 730-731; Escudero et al. 2012, p. 362; 
Espoz et al. 2008, p. 74; Niles et al. 2008, p. 101; also see 
Asynchronies, below). Due to harvest restrictions and other 
conservation actions, horseshoe crab populations showed some signs of 
recovery in the early 2000s, with apparent signs of red knot 
stabilization (survey counts, rates of weight gain) occurring a few 
years later (as might be expected due to biological lag times). Since 
about 2005, however, horseshoe crab population growth has stagnated for 
unknown reasons.
    Under the current management framework (known as Adaptive Resource 
Management, or ARM), the present horseshoe crab harvest is not 
considered a threat to the red knot because harvest levels are tied to 
red knot populations via scientific modeling. Most data suggest that 
the volume of horseshoe crab eggs is currently sufficient to support 
the Delaware Bay's stopover population of red knots at its present 
size. However, because of the uncertain trajectory of horseshoe crab 
population growth, it is not yet known if the egg resource will 
continue to adequately support red knot populations over the next 5 to 
10 years. In addition, implementation of the ARM could be impeded by 
insufficient funding for the shorebird and horseshoe crab monitoring 
programs that are necessary for the functioning of the ARM models.

[[Page 60064]]

    Many studies have established that red knots stopping over in 
Delaware Bay during spring migration achieve remarkable and important 
weight gains to complete their migrations to the breeding grounds by 
feeding almost exclusively on a superabundance of horseshoe crab eggs 
(see the ``Wintering and Migration Food'' section of the Rufa Red Knot 
Ecology and Abundance supplemental document). A temporal correlation 
occurred between increased horseshoe crab harvests in the 1990s and 
declining red knot counts in both Delaware Bay and Tierra del Fuego by 
the 2000s. Other shorebird species that rely on Delaware Bay also 
declined over this period (Mizrahi and Peters in Tanacredi et al. 2009, 
p. 78), although some shorebird declines began before the peak 
expansion of the horseshoe crab fishery (Botton et al. in Shuster et 
al. 2003, p. 24).
    The causal chain from horseshoe crab harvest to red knot 
populations has several links, each with different lines of supporting 
evidence and various levels of uncertainty: (a) Horseshoe crab harvest 
levels and Delaware Bay horseshoe crab populations (Link A); (b) 
horseshoe crab populations and red knot weight gain during the spring 
stopover (Link B); and (c) red knot weight gain and subsequent rates of 
survival, reproduction, or both (Link C). The weight of evidence 
supporting each of these linkages is discussed below. Despite the 
various levels of uncertainty, the weight of evidence supports these 
linkages, points to past harvest as a key factor in the decline of the 
red knot, and underscores the importance of continued horseshoe crab 
management to meet the needs of the red knot.
Horseshoe Crab--Harvest and Population Levels (Link A)
    Historically, horseshoe crabs were harvested commercially for 
fertilizer and livestock feed. From the mid-1800s to the mid-1900s, 
harvest ranged from about 1 to 5 million crabs annually. Harvest 
numbers dropped to 250,000 to 500,000 crabs annually in the 1950s, 
which are considered the low point of horseshoe crab abundance. Only 
about 42,000 crabs were reported annually by the early 1960s. Early 
harvest records should be viewed with caution due to probable 
underreporting. The substantial commercial-scale harvesting of 
horseshoe crabs ceased in the 1960s (ASMFC 2009, p. 1). By 1977, the 
spawning population of horseshoe crabs in Delaware Bay was several 
times larger than during the 1960s, but was far from approaching the 
numbers and spawning intensity reported in the late 1800s (Shuster and 
Botton 1985, p. 363). No information is available on how these 
historical harvests of horseshoe crabs may have affected populations of 
red knots or other migratory shorebirds, but these historical harvests 
occurred at a time when shorebird numbers had also been markedly 
reduced by hunting (Botton et al. in Shuster et al. 2003, pp. 25-26; 
Dunne in New Jersey Audubon Society 2007, p. 25); see Factor B, above.
    During the 1990s, reported commercial harvest of horseshoe crabs on 
the Atlantic coast of the United States increased dramatically. Modern 
harvests are for bait and the biomedical industry. Commercial fisheries 
for horseshoe crab consist primarily of directed trawls and hand 
harvest (e.g., collection from beaches during spawning) (ASMFC 2009, p. 
14). Horseshoe crabs are used as bait in the American eel (Anguilla 
rostrata), conch (whelk) (Busycon spp.), and other fisheries. The 
American eel pot fishery prefers egg-laden female horseshoe crabs, 
while the conch pot fishery uses both male and female horseshoe crabs. 
The increase in harvest of horseshoe crabs during the 1990s was largely 
due to increased use as conch bait (ASMFC 2009, p. 1).
    Although also used in scientific research and for other medical 
purposes, the major biomedical use of horseshoe crabs is in the 
production of Limulus Amebocyte Lysate (LAL). The LAL is a clotting 
agent in horseshoe crab blood that makes it possible to detect human 
pathogens in patients, drugs, and intravenous devices (ASMFC 2009, p. 
2). The ``LAL test'' is currently the worldwide standard for screening 
medical equipment and injectable drugs for bacterial contamination 
(ASMFC 2009, p. 2; ASMFC 1998, p. 12). Horseshoe crab blood is obtained 
from adult crabs that are released alive after extraction is complete 
(ASMFC 2009, p. 2) or that are sold into the bait market (ASMFC 2009, 
p. 18). The ASMFC previously assumed a constant 15 percent mortality 
rate for bled crabs that are not turned over to the bait fishery (ASMFC 
2009, p. 3) but now considers a range from 5 to 30 percent mortality 
(ASMFC 2012a, p. 6) more appropriate. The estimated mortality rate 
includes all crabs rejected for biomedical use any time between capture 
and release.
    Bait harvest and biomedical collection have been managed separately 
by the ASMFC since 1999 (ASMFC 1998, pp. iii-57). Biomedical collection 
is currently not capped, but ASMFC considers implementing action to 
reduce mortality if estimated mortality exceeds a threshold of 57,500 
crabs. This threshold has been exceeded several times, but thus far the 
ASMFC has opted only to issue voluntary guidelines to the biomedical 
industry (ASMFC 2009, p. 18). The ASMFC implemented key reductions in 
the bait harvest in 2000, 2004, and 2006 (ASMFC 2009, p. 3), and 
several member States have voluntarily restricted harvests below their 
allotted quotas (ASMFC 2012a, pp. 4, 13; N.J.S.A. 23:2B-21; N.J.R. 
2139(a)). Along with the widespread use of bait-saving devices, these 
restrictions reduced reported landings (ASMFC 2009, p. 1) from 1998 to 
2011 by over 75 percent (table 9). Further, a growing number of 
horseshoe crabs are being biomedically bled first before being used as 
bait; because such crabs count against harvest quotas (ASMFC 2012a, p. 
6), this practice helps reduce total mortality rates. In addition, the 
National Marine Fisheries Service (NMFS) established the Carl N. 
Shuster Jr. Horseshoe Crab Reserve in 2001, as recommended by the 
ASMFC. About 30 nautical miles (55.6 km) in radius and located in 
Federal waters off the mouth of the Delaware Bay, the reserve is closed 
to commercial horseshoe crab harvest except for limited biomedical 
collection authorized periodically by NMFS (NOAA 2001, pp. 8906-8911).
    Evidence that commercial harvests caused horseshoe crab population 
declines in recent decades comes primarily from a strong temporal 
correlation between harvest levels (as measured by reported landings, 
tables 8 and 9) and population levels (as characterized by ASMFC during 
stock assessments).
Link A, Part 1--Horseshoe Crab Harvest Levels
    The horseshoe crab landings given in pounds in tables 8 and 9 come 
from data reported to NMFS, but should be viewed with caution as these 
records are often incomplete and represent an underestimate of actual 
harvest (ASMFC 1998, p. 6). In addition, reporting has increased over 
the years, and the conversion factors used to convert crab numbers to 
pounds have varied widely. Despite these inaccuracies, the reported 
landings show that commercial harvest of horseshoe crabs increased 
substantially from 1990 to 1998 and has generally declined since then 
(ASMFC 2009, p. 2). The ASMFC (1998, p. 6) also considered other data 
sources to corroborate a significant increase in harvest in the 1990s. 
These landings (pounds) may include biomedical collection, live trade, 
and bait fishery harvests (ASMFC 2009, p. 17).
    Table 9 also shows the number of crabs harvested for bait, and the

[[Page 60065]]

estimated number of crabs killed incidental to biomedical collection, 
as reported to ASMFC. Since 1998, States have been required to report 
annual bait landings to ASMFC, which considers these data reliable 
(ASMFC 2009, p. 2). A subtotal of the bait harvest is shown for the 
Delaware Bay Region (New Jersey, Delaware, and a part of the harvests 
in Maryland and Virginia), as managed by ASMFC. The numbers given in 
tables 8 and 9 do not reflect the changing sex ratio of crabs harvested 
in the Delaware Bay Region (S. Michels pers. comm. February 15, 2013), 
which has shifted away from the harvest of females since management 
began. In 2013, the first year that the harvest level was determined 
using the ARM, the quota in the Delaware Bay Region is set at 500,000 
males and 0 females (ASMFC 2012b, p. 1); however, we do not yet have 
access to the actual number of crabs removed in 2013 to compare against 
the quota. Since 2006, all four States in the Delaware Bay Region have 
frequently harvested fewer crabs than allowed by the ASMFC (ASMFC 
2012a, p. 13). From 2006 to 2011, New Jersey opted not to use its 
100,000-crab quota by imposing a moratorium, which the State is now 
considering lifting amid considerable controversy between environmental 
and fishing groups (Augenstein 2013, entire; ASMFC 2012a, p. 13; 
N.J.S.A. 23:2B-21; N.J.R. 2139(a)).
    Estimates of biomedical collection increased from 130,000 crabs in 
1989 to 260,000 in 1997 (ASMFC 2004, p. 12). Since mandatory reporting 
requirements took effect in 2004, biomedical-only crabs collected 
(i.e., crabs not counted against State bait harvest quotas) rose from 
292,760 in 2004 (ASMFC 2009, pp. 18, 41) to 545,164 in 2011 (ASMFC 
2012a, p. 6). Total estimated mortality of biomedical crabs for 2011 
was 80,827 crabs (using a 15 percent post-release estimated mortality; 
see table 9), with a range of 31,554 to 154,737 crabs (using 5 to 30 
percent estimated mortality) (ASMFC 2012a, p. 6). Using a constant 15 
percent mortality of bled crabs, the estimated contribution of 
biomedical collection to total (biomedical plus bait) mortality rose 
from about 6 percent in 2004 to about 11 percent in 2011.
    To put the reported harvest numbers in context, two recent 
assessments using different methods both estimated the population of 
horseshoe crabs in the Delaware Bay Region at about 20 million adults, 
with approximately twice as many males as females (Sweka pers. comm. 
May 30, 2013; Smith et al. 2006, p. 461). Therefore, recent annual 
harvests of roughly 200,000 horseshoe crabs from the Delaware Bay 
Region represent about 1 percent of the adult population.

                 Table 8--Reported Atlantic Coast Horseshoe Crab Landings (Pounds), 1970 to 2011
                                                  [NOAA 2012d]
                                                              Total pounds                        Total pounds
                           Year                             reported to NMFS        Year        reported to NMFS
1970......................................................            15,900              1991           385,487
1971......................................................            11,900              1992           321,995
1972......................................................            42,000              1993           821,205
1973......................................................            88,700              1994         1,171,571
1974......................................................            16,700              1995         2,416,168
1975......................................................            62,800              1996         5,159,326
1976......................................................         2,043,100              1997         5,983,033
1977......................................................           473,000              1998         6,835,305
1978......................................................           728,500              1999         5,246,598
1979......................................................         1,215,630              2000         3,756,475
1980......................................................           566,447              2001         2,336,645
1981......................................................           326,695              2002         2,772,010
1982......................................................           526,700              2003         2,624,248
1983......................................................           468,600              2004           974,425
1984......................................................           225,112              2005         1,421,957
1985......................................................           614,939              2006         1,548,900
1986......................................................           635,823              2007         1,804,968
1987......................................................           511,758              2008         1,315,963
1988......................................................           688,839              2009         1,830,506
1989......................................................         1,106,645              2010           869,630
1990......................................................           519,057              2011         1,497,462

            Table 9--Reported Atlantic Coast Horseshoe Crab Landings (Pounds and Crabs), 1998 to 2011
[(A. Nelson Pers. Comm. February 22, 2013 and November 27, 2012; ASMFC 2012a, pp. 6, 13; NOAA 2012d; ASMFC 2009,
                                       pp. 38-41); ND = No Data Available]
                                                                                                   numbers of
                                                                                                 crabs killed by
                                                                              Numbers of crabs     biomedical
                                                            Numbers of crabs    harvested for      collection,
                                            Total pounds      harvested for   bait reported to     based on 15
                  Year                    reported to NMFS  bait reported to  ASMFC,  Delaware   percent of  the
                                            (from Table 8)        ASMFC          Bay  Region          total
                                                                                  subtotal         biomedical
                                                                                                   reported to
1998....................................         6,835,305         2,748,585           862,462                ND
1999....................................         5,246,598         2,600,914         1,013,996                ND
2000....................................         3,756,475         1,903,415           767,988                ND

[[Page 60066]]

2001....................................         2,336,645         1,013,697           607,602                ND
2002....................................         2,772,010         1,265,925           728,266                ND
2003....................................         2,624,248         1,052,493           584,394                ND
2004....................................           974,425           681,323           278,280            45,670
2005....................................         1,421,957           769,429           347,927            44,830
2006....................................         1,548,900           840,944           270,241            49,182
2007....................................         1,804,968           827,554           169,255            63,432
2008....................................         1,315,963           660,794           190,828            63,285
2009....................................         1,830,506           756,484           250,699            60,642
2010....................................           869,630           604,548           165,852            75,428
2011....................................         1,497,462           650,539           195,153            80,827

Link A, Part 2--Horseshoe Crab Population Levels
    Through stock assessments, ASMFC analyzes horseshoe crab data from 
many different independent surveys and models (ASMFC 2004, pp. 14-24; 
ASMFC 2009, pp. 14-23). In the 2004 assessment, ASMFC found a clear 
preponderance of evidence that horseshoe crab populations in the 
Delaware Bay Region declined from the late 1980s to 2003, and that 
declines early in this evaluation period were steeper than later 
declines (ASMFC 2004, p. 27). Genetic analysis also suggested that the 
Delaware Bay horseshoe crab population was exhibiting the effects of a 
recent population bottleneck in the mid-1990s (Pierce et al. 2000, pp. 
690, 691, 697), and modeling confirmed that overharvest caused declines 
(Smith et al. in Tanacredi et al. 2009, p. 361). In the 2009 stock 
assessment, ASMFC concluded that there was no evidence of ongoing 
declines in the Delaware Bay Region, and that the demographic pattern 
of significant increases matched the expectations for a recovering 
population (ASMFC 2009, p. 23). These findings support the temporal 
correlation that rising harvest levels led to population declines 
through the 1990s, while management actions had started reversing the 
decline by the mid-2000s.
    Though no formal horseshoe crab stock assessment has been conducted 
since 2009, the ASMFC's Delaware Bay Ecosystem Technical Committee 
recently reviewed current data from the same trawl and dredge surveys 
that were evaluated in the 2004 and 2009 assessments. From these data, 
the committee concluded that declines were observed during the 1990s, 
stabilization occurred in the early 2000s, various indicators have 
differed with no consistent trends since 2005, confidence intervals are 
large, there is no clear trend apparent in recent data, and the 
population has at least stabilized (ASMFC 2012c, pp. 10-12). These 
conclusions generally support the link between harvest levels and 
available indicators of horseshoe crab abundance. The committee noted, 
however, that sustained horseshoe crab population increases have not 
been realized as expected. The reasons for this stagnation are unknown, 
and a recent change in sex ratios is also unexplained (i.e., several 
surveys found that the ratio of males to females increased sharply 
since 2010 despite several years of reduced female harvests) (S. 
Michels pers. comm. February 15, 2013; ASMFC 2012d, pp. 17-18; ASMFC 
2010, pp. 2-3). The committee speculated that some combination of the 
following factors may explain the lack of recent population growth, but 
committee members did not reach consensus regarding which factors are 
more likely (ASMFC 2012c, p. 12; ASMFC 2012d, p. 2).
     Insufficient time since management actions were taken. 
There would likely be at least a 10-year time lag between fishery 
restrictions and significant population changes, corresponding to the 
horseshoe crab's estimated age at sexual maturity (Sweka et al. 2007, 
p. 285; ASMFC 2004, p. 31). Based on modeling, Davis et al. (2006, p. 
222) found that the horseshoe crab population in the Delaware Bay 
Region had been depleted and harvest levels at that time may have been 
too high to allow the population to rebuild within 15 years. The most 
recent harvest reductions were implemented in 2006 (ASMFC 2009, p. 3; 
38 N.J.R. 2139(a)).
     An early life-history (recruitment) bottleneck. Sweka et 
al. (2007, pp. 277, 282, 284) found that early-life-stage mortality, 
particularly mortality during the first year of life, was the most 
important parameter affecting modeled population growth, and that 
estimates of egg mortality have high uncertainty.
     Undocumented or underestimated mortality.
    [cir] One possible source of error is the use of a constant 15 
percent mortality for biomedically bled crabs. Leschen and Correia 
(2010a, p. 135) reported mortality rates of nearly 30 percent, although 
this result has been disputed (Dawson 2010, pp. 2-3; Leschen and 
Correia 2010b, pp. 8-10). The ASMFC now considers a range from 5 to 30 
percent mortality (ASMFC 2012a, p. 6).
    [cir] Poaching may be another factor, as documented by enforcement 
actions in New Jersey (Mucha 2011) and New York (Goodman 2013; Randazzo 
2013; J. Gilmore pers. comm. October 24, 2012). The New Jersey incident 
was small, and no other violations are known to have occurred in New 
Jersey (D. Fresco pers. comm. November 9, 2012). Although the poaching 
in New York involved substantial numbers of crabs, New York waters are 
outside the Delaware Bay Region and should not affect population

[[Page 60067]]

trends in this Region. Together, though, these incidents hint that 
illegal harvest may be a factor, although the ASMFC law enforcement 
committee reported very few problems or issues in the past few years 
(M. Hawk pers. comm. April 29, 2013).
    [cir] The harvest of horseshoe crabs from Federal waters that are 
not landed in any state, but exchanged directly to a dependent fishery, 
is unregulated, and, therefore, the magnitude of any such harvest is 
unknown (ASMFC 1998, p. 27). However, there is no evidence that such 
boat-to-boat transfers are occurring, and the level of any such 
unreported harvest is thought to be small and unlikely to have 
population-level effects (M. Hawk pers. comm. April 29, 2013; G. Breese 
pers. comm. April 26, 2013).
    [cir] The extent of horseshoe crab mortality due to bycatch from 
other fisheries is unknown (ASMFC 1998, pp. 22, 26); however, at least 
one State does regulate and limit such bycatch (Virginia Marine 
Resources Commission Chapter 4 VAC 20-900-10 et. seq.), and horseshoe 
crabs caught as bycatch in the Carl N. Shuster Jr. Horseshoe Crab 
Reserve must be returned to the water (NOAA 2001, p. 8906).
     Limitations in the ability of surveys to capture trends. 
Inherent variability in most of the data sets decreases the predictive 
power of the surveys, especially over short time periods. For the 
majority of horseshoe crab indices, detecting small changes in 
population size would require 10 to 15 years of data. Over the short 
term, these indices would be able to identify only a catastrophic 
decline in the horseshoe crab population (ASMFC 2004, p. 31).
     An ecological shift. Examples are available from other 
fisheries, such as weakfish (Cynoscion regalis). The weakfish quota was 
dramatically cut, but the population never rebounded. Despite some 
years of excellent recruitment, adult weakfish stocks have not 
recovered perhaps due to increased predation (S. Doctor pers. comm. 
November 8, 2012). Changes in predation, competition, or other 
ecological factors can cause a population to stabilize at a new, lower 
    In addition to the aforementioned potential causes for lack of 
recent growth in horseshoe crab populations, threats to horseshoe crab 
spawning habitat are discussed under Factor A above. Another potential 
threat to horseshoe crab populations recently emerged--the proposed 
importation of nonnative horseshoe crab species for use as bait. 
Nonnative species could carry diseases and parasites that could put the 
native species at risk, and exports to the U.S. bait market could 
hasten declines in the Asian species, which is discussed below. The 
Service currently lacks the regulatory authority to restrict the 
importation of these species on the Federal level (i.e., under the 
Lacey Act, see supplemental document--Factor D), although Congress is 
deliberating legislation to expand that authority (USFWS 2013, pp. 1-
2). In the meantime, ASMFC has recommended that all member States ban 
the import and use of Asian horseshoe crabs as bait in State water 
fisheries along the Atlantic coast (ASMFC 2013, entire), although no 
such State bans have yet gone into effect.
    Asian horseshoe crab species are themselves in decline (ASMFC 2013, 
p. 2), and their status could indirectly affect the American species. 
Chinese scientists have reported rapid growth in biomedical collection 
and correspondingly rapid population declines in harvested populations. 
Anecdotal observations and predictions from scientists close to the 
industry suggest that such harvest is unsustainable. If the Asian 
biomedical industry were to collapse due to exhausted stocks of these 
species, then the worldwide demand for amebocyte lysate would be 
focused on the American horseshoe crab alone, potentially increasing 
biomedical collection pressure in the United States (Smith and Millard 
2011, p. 1). However, research is being conducted on substitutes for 
LAL (PhysOrg 2011; Janke 2008, entire; Chen 2006, entire) and on 
artificial bait for the conch and eel fisheries (Bauers 2013b; Ferrari 
and Targett 2003, entire). If successful, any such developments could 
reduce or eliminate the demand for harvesting horseshoe crabs.
Horseshoe Crab--Crab Population and Red Knot Weight Gain (Link B)
    Attempts have generally not been made to tie weight gain in red 
knots during the spring stopover to the total horseshoe crab population 
size in the Delaware Bay Region. Instead, most studies have looked for 
correlations between red knot weight gain and either the abundance of 
spawning horseshoe crabs, or the density of horseshoe crab eggs in the 
top 2 in (5 cm) of sediment (within the reach of the birds). Other 
studies provide information regarding trends in egg sufficiency and red 
knot weight gain over time.
Link B, Part 1--Horseshoe Crab Spawning Abundance
    A baywide horseshoe crab spawning survey has been conducted under 
consistent protocols since 1999. Based on data through 2011, numbers of 
spawning females have not increased or decreased, while numbers of 
spawning males showed a statistically significant increase. Though not 
statistically significant, female crab trends were negative in Delaware 
and positive in New Jersey (Zimmerman et al. 2012, pp. 1-2). The ASMFC 
Delaware Bay Ecosystem Technical Committee recently questioned whether 
the spawning survey has reached ``saturation'' levels, at which 
appreciable increases in spawning crab numbers may not be detected 
under the current survey design. The committee is investigating this 
question (ASMFC 2012d, p. 7).
    Strong evidence for a link between numbers of spawning crabs and 
red knot weight gain comes from the modeling that underpins the ARM. 
The probability that a bird arriving at Delaware Bay weighing less than 
6.3 oz (180 g) will attain a weight of greater than 6.3 oz (180 g) was 
positively related to the estimated female crab abundance on spawning 
beaches during the migration stopover (McGowan et al. 2011a, p. 12).
Link B, Part 2--Horseshoe Crab Egg Density
    Due to the considerable vertical redistribution (digging up) of 
buried eggs (4 to 8 in (10 to 20 cm) deep) by waves and further 
spawning activity, surface egg densities (in the top 2 in (5 cm) of 
sediment) are not necessarily correlated with the density of spawning 
horseshoe crabs (Smith et al. 2002b, p. 733). Therefore, egg density 
surveys are not meant as an index of horseshoe crab abundance. Instead, 
attempts have been made to use the density of eggs in the top few 
inches of sediment as an index of food availability for shorebirds (Dey 
et al. 2013, p. 8), for example by correlating these egg densities with 
red knot weight gain.
    Egg density surveys were conducted in New Jersey in 1985, 1986, 
1990, and 1991, and annually since 1996. Surveys have been carried out 
in Delaware since 1997. Methodologies have evolved over time, but have 
been relatively consistent since 2005. Direct comparisons between New 
Jersey and Delaware egg density data are inappropriate due to 
differences in survey methodology between the two States, despite 
standardization efforts (ASMFC 2012d, pp. 11-12; Niles et al. 2008, pp. 
33, 44, 46).
    Niles et al. (2008, p. 45) reported egg densities from 1985, 1986, 
1990, and 1991 an order of magnitude higher than for the period 
starting in 1996. Conversion factors were developed to

[[Page 60068]]

allow for comparison between the 1985 to 1986 and the 1990 to 1991 data 
points (Niles et al. 2008, p. 44), and statistical analysis found that 
data points from 2000 to 2004 can be directly compared to those from 
2005 to 2012 without a conversion factor (i.e., a 2005 change in 
sampling method did not affect the egg density results) (Dey et al. 
2011b, p. 12). However, comparisons between the earlier data points 
(1985 to 1999) and egg densities since 2000 are confounded by changes 
in methodology and investigators, and lack of conversion factors.
    Higher confidence is attached to trends since 2005 because 
methodologies have been consistent over that period. The ASMFC's 
Delaware Bay Ecosystem Technical Committee recently reviewed the most 
current egg density data from both States. The committee concluded 
there was no significant trend in baywide egg densities from 2005 to 
2012. Looking at the two States separately, Delaware showed no 
significant trend in egg density, while the trends in New Jersey were 
positive. Markedly higher egg densities on some beaches (e.g., 
Mispillion Harbor, Delaware and Moores Beach, New Jersey) strongly 
influence Statewide and baywide trends. These higher densities 
predictably occur in a few locations (ASMFC 2012d, p. 9). If one of 
these high-density beaches is excluded (Mispillion Harbor), Delaware 
shows a negative trend from 2005 to 2012 (A. Dey pers. comm. October 
12, 2012).
    Using data from 2005 to 2012, Dey et al. (2013, pp. 8, 18) found a 
statistically strong relationship between the proportion of red knots 
reaching the estimated optimal departure weight (6.3 oz (180 g) or 
more) from May 26 to 28, and the baywide median density of horseshoe 
crab eggs, excluding Mispillion Harbor, during the third and fourth 
weeks of May. This statistical relationship suggests that the egg 
survey data may provide a reasonable measure of egg availability and 
its link to red knot weight gain (ASMFC 2012d, p. 11). However, the 
exclusion of Mispillion Harbor is problematic because egg densities at 
this site are an order of magnitude higher than at other beaches (Dey 
et al. 2013, pp. 10, 14); Mispillion Harbor has supported large numbers 
of red knots even in years when the measure of baywide egg densities 
has been low, consistently containing upwards of 15 to 20 percent of 
all the knots recorded in Delaware Bay (Lathrop 2005, p. 4). A 
mathematical relationship between egg densities and red knot departure 
weights holds with the addition of Mispillion Harbor, but is 
statistically weaker (Dey et al. 2013, pp. 18-19; H. Sitters pers. 
comm. April 26, 2013). In addition, problems have been noted with both 
the egg density surveys and the characterization of red knot weights 
relative to particular dates; each are discussed below.
    Regarding the egg surveys, samples are similarly collected across 
the bay, but egg separation and counting methodologies are 
substantially different between New Jersey and Delaware and have not 
been fully documented in either State. In addition, very high spatial 
and temporal variability in surface egg densities limits the 
statistical power of the surveys (ASMFC 2012d, p. 11). Based on the 
sampling methodology used in both States (Dey et al. 2011b, pp. 3-4), 
the surveys would be expected to have only about a 75 percent chance of 
detecting a major (50 percent) decline in egg density over 5 years 
(Pooler et al. 2003, p. 700). In addition, the sampled segments on a 
particular beach may not be representative of egg densities throughout 
that larger beach (Pooler et al. 2003, p. 700) and may not reflect the 
red knots' preferential feeding in microhabitats where eggs are 
concentrated, such as at horseshoe crab nests (Fraser et al. 2010, p. 
99), the wrack line (Karpanty et al. 2011, p. 990; Nordstrom et al. 
2006a, p. 438), and shoreline discontinuities (Botton et al. 1994, p. 
    Data on the proportion of birds caught at 6.3 oz (180 g) or greater 
from May 26 to 28 should also be interpreted with caution (Dey et al. 
2011a, p. 7). The proportion of the whole stopover population that is 
present in the bay and available to be caught and weighed from May 26 
to 28 varies from year to year. In addition, the late May sampling 
event cannot take account of those birds that achieve adequate mass and 
either depart Delaware Bay early (Dey et al. 2011a, p. 7) or spend more 
time roosting away from the capture sites (which are located in 
foraging areas) (Robinson et al. 2003, p. 11). The fact that birds 
arrive and depart the stopover area at different times can also 
confound attempts to calculate weight gain over the course of the 
stopover season, underestimating the gains by as much as 30 to 70 
percent (Gillings et al. 2009, pp. 55, 59; Zwarts et al. 1990, p. 352). 
Modeling for the ARM produced a strong finding that the probability of 
capturing light birds (less than 6.3 oz; 180 g) is considerably higher 
(0.071) than of capturing heavy birds (greater than 6.3 oz; 180 g) 
(0.019) (McGowan et al. 2011a, p. 8). In addition, a single target 
weight and date for departure is likely an oversimplification; while 
likely to hold true for the population average, individual birds likely 
employ diverse ``strategies'' for departure date and weight influenced 
by the bird's size, condition, arrival date, and other factors 
(Robinson et al. 2003, p. 13).
    Despite the high uncertainty of the egg density data and a known 
bias in recorded red knot weights, these metrics do show a significant 
positive correlation to one another, and we have, therefore, considered 
this information. Although the birds captured and weighed at the end of 
May are very likely lighter than the population-wide average departure 
weight, these birds may represent a useful index of late-departing 
knots that may be particularly dependent on a superabundance of 
horseshoe crab eggs (see Asynchronies, below).
Link B, Part 3--Trends in Horseshoe Crab Egg Sufficiency
    Looking at the duration that shorebirds spent in Delaware Bay early 
versus late in the stopover period, Wilson (1991, pp. 845-846) 
concluded there was no evidence of food depletion, but he did not 
account for time constraints that late-arriving birds may face. In 1990 
and 1991, Botton et al. (1994, pp. 612-613) found that all but one of 
the seven beaches sampled were capable of supporting at least four 
birds per 3.3 ft (1 m) of shoreline, and the supply of eggs was 
sufficient to accommodate the number of birds using these beaches at 
that time.
    By 2002 and 2003, Gillings et al. (2007, p. 513) found that few 
beaches provided high enough densities of buried eggs (2 to 8 in (5 to 
20 cm) deep) for rapid egg consumption (i.e., through vertical 
redistribution, as discussed above), making birds dependent on a 
smaller number of sites where conditions were suitable for surface 
deposition (e.g., from the receding tide). Comparing survey data from 
1992 and 2002, usage of Delaware Bay by foraging gulls declined despite 
growing regional gull populations, another indication that birds were 
responding to reduced availability of horseshoe crab eggs around 2002 
(Sutton and Dowdell 2002, p. 6). Based on models of red knot foraging 
responses observed in 2003 and 2004, Hernandez (2005, p. 35) estimated 
egg densities needed to optimize foraging efficiency, and these 
estimates were generally consistent with requisite egg densities 
calculated by Haramis et al. (2007, p. 373) based on captive red knot 
feeding trials. These studies suggested that available egg densities in 
the early 2000s may have been insufficient for red knots to meet their 
energetic requirements (Niles et al.

[[Page 60069]]

2008, pp. 36-39). A geographic contraction of red knots into fewer 
areas of Delaware Bay may have also indicated egg insufficiency. From 
1986 to 1990, red knots were relatively evenly distributed along the 
Delaware Bay shoreline in both New Jersey and Delaware. In comparison, 
there was a much greater concentration of red knots in the fewer areas 
of high horseshoe crab spawning activity from 2001 to 2005 (Lathrop 
2005, p. 4). In 2004, Karpanty et al. (2006, p. 1706) found that only 
about 20 percent of the Delaware Bay shoreline contained enough eggs to 
have a greater than 50 percent chance of finding red knots, and that 
red knots attended most or all of the available egg concentrations.
    Newer evidence suggests that the apparent downward trend in egg 
sufficiency may have stabilized by the mid-2000s. In 2004 and 2005, 
Karpanty et al. (2011, p. 992) found that eggs became depleted in the 
wrack line, but also found several other lines of evidence that egg 
numbers were sufficient for the red knot stopover populations present 
in those years. This evidence included egg counts over time, bird 
foraging rates and behaviors, egg exclosure experiments, and lack of 
competitive exclusion (Karpanty et al. 2011, p. 992).
Link B, Part 4--Trends in Red Knot Weight Gain
    From 1997 to 2002, Baker et al. (2004, p. 878) found that an 
increasing proportion of red knots, particularly those birds that 
arrived late in Delaware Bay, failed to reach threshold departure 
masses of 6.3 to 7.1 oz (180 to 200 g). Despite using a slightly 
different target weight and departure date, Atkinson et al. (2003b, p. 
3) had reached the same conclusion that, relative to 1997 and 1998, an 
increasing proportion of birds failed to reach target weights through 
2002. Modeling conducted by Atkinson et al. (2007, p. 892) suggested 
that, due to poor foraging and weather conditions, red knot fueling 
(temporal patterns and rates of weight gain) proceeded as normal from 
1997 to 2002, except in 2000, but not in 2003 or 2005.
    Dey et al. (2011a, p. 6) found a significant quadratic (a 
mathematical relationship between one variable and the square of 
another variable) relationship between the percent of red knots 
weighing 6.3 oz (180 g) or more in late May (May 26 to 28) and time 
(1997 to 2011). The strength of the quadratic relationship owes much to 
the very low proportion (0 percent) of heavy birds in 2003, but it is 
still significant if the 2003 data are omitted. This relationship holds 
with the addition of 2012 data and shows a downward trend in the 
percent of heavy birds since 1997, which started to reverse by the late 
2000s; however, the percent of heavy birds in late May has not yet 
returned to 1990s levels (A. Dey pers. comm. October 12, 2012).
    It is noteworthy that the downward trend in the percent of late-May 
heavy birds appears to have leveled off around 2005 (A. Dey pers. comm. 
October 12, 2012), around the same time that Karpanty et al. (2011, p. 
992) found evidence of sufficient horseshoe crab eggs, and following 
the period of horseshoe crab population growth (ASMFC 2012c, pp. 10-12) 
that was discussed under Population Levels (Link A, Part 2), above. 
Peak counts of red knots in Delaware Bay have also been generally 
stable since approximately this same time (A. Dey pers. comm. October 
12, 2012; Dey et al. 2011a, p. 3), although at a markedly reduced 
level. These lines of evidence suggest that the imminent threat of egg 
insufficiency was stabilized, though not fully abated, around 2005. 
Because of the uncertain trajectory of horseshoe crab population growth 
since 2005, it is not yet known if the egg resource will continue to 
adequately support red knot populations in the future.
Horseshoe Crab--Red Knot Weight Gain and Survival/Reproduction (Link C)
    In the causal chain from horseshoe crab harvest to red knot 
populations, the highest uncertainty is associated with the link 
between red knot weight gain at the Delaware Bay in May and the birds' 
survival, reproduction, or both, during the subsequent breeding season. 
Using data from 1997 to 2002 and slightly different target departure 
dates (May 31) and weights (6.9 oz (195 g)), early modeling by Atkinson 
et al. (2003b, pp. 15-16) found support for the hypothesis that birds 
with lower departure weights have lower survival rates and that 
survival rates apparently decreased over this time. Demonstrating the 
importance of the stopover timing (see Asynchronies, below), survival 
rates of birds caught from May 10 to May 20 did not seem to change from 
1997 to 2002, and was consistently high. However, for birds caught 
after May 20, the range of survival rates was much wider, and birds 
were predicted to have higher mortality rates (Atkinson et al. 2003b, 
p. 16).
    More recently, two benchmark studies have attempted to measure the 
strength of the relationship between departure weight from Delaware Bay 
and subsequent survival using mathematical models. By necessity, this 
type of modeling relies on numerous assumptions, which increases 
uncertainty in the results. Both studies took advantage of the 
extensive body of red knot field data, which makes the models more 
robust than would be possible for less well-studied species. 
Nevertheless, the two modeling efforts produced somewhat inconsistent 
    Baker et al. (2004, pp. 878-897) found that average annual survival 
declined significantly from an average of 85 percent from 1994 to 1998 
to 56 percent from 1998 to 2001. Linking weight gain to survival, Baker 
et al. (2004, p. 878) found that red knots known to survive to a later 
year, through recaptures or resightings throughout the flyway, were 
heavier at initial capture than birds never seen again. According to 
Baker et al. (2004, entire), mean predicted body mass of known 
survivors was greater than 6.3 oz (180 g) in each year of the study (as 
cited in McGowan et al. 2011a, p. 14).
    Using data from 1997 to 2008, McGowan et al. (2011a, p. 13) found 
considerably higher survival rates (around 92 percent) than Baker et 
al. (2004, entire) had reported. McGowan et al. (2011a, p. 9) did 
confirm that heavy birds had a higher average survival probability than 
light birds, but the difference was small (0.918 versus 0.915). Based 
on the work of Baker et al. (2004), McGowan et al. (2011a, p. 13) had 
expected a larger difference in survival rates between heavy and light 
    However, the average survival rate (1997 to 2008) can mask 
differences among years. Looking at these temporal differences, the 
findings of McGowan et al. (2011a, entire) were more consistent with 
Baker et al. (2004, entire), and McGowan's year-specific survival rate 
estimates for 1997 to 2002 fell within the ranges presented by Baker et 
al. (2004). McGowan's lowest survival estimates occurred in 1998, just 
before the period of sharpest declines in red knot counts (McGowan et 
al. 2011a, p. 13) (see supplemental document--Rufa Red Knot Ecology and 
Abundance--tables 2 and 10). Also, the survival of light birds was 
lower than heavy birds in 6 of the 11 years analyzed. For example, the 
1998 to 1999 survival rate estimate was 0.851 for heavy birds and only 
0.832 for light birds (McGowan et al. 2011a, p. 9). Finally, McGowan et 
al. (2011a, p. 14) noted that the data presented by Baker et al. (2004) 
show survival rates increased during 2001 and 2002. These points of 
comparison between the two studies suggest that the years of the Baker 
et al. (2004, entire) study may have corresponded to the period of 
sharpest red knot declines that

[[Page 60070]]

have subsequently begun to stabilize. Stabilization around the mid-
2000s is also supported by several other lines of evidence, as 
discussed under Trends in Red Knot Weight Gain (Link B, Part 4), above. 
However, McGowan et al. (2011a, p. 14) suggested several possible 
methodological reasons why their results differed from Baker et al. 
(2004, entire); primarily, that the newer study attempted to account 
for the known bias toward capturing lighter birds.
    McGowan et al. (2011b, entire) simulated population changes of 
horseshoe crabs and red knots using reported horseshoe crab harvest 
from 1998 to 2008 and the red knot survival and mass relationships 
reported by McGowan et al. (2011a). These tests demonstrated that the 
survival estimates reported by McGowan et al. (2011a) are potentially 
consistent with a projected median red knot population decline of over 
40 percent (McGowan et al. 2011a, p. 13), over the same period in which 
declining counts were recorded in both Delaware Bay and Tierra del 
    A line of corroborating evidence comes from the demonstration of 
similar linkages in other Calidris canutus subspecies. For example, 
Morrison (2006, pp. 613-614) and Morrison et al. (2007, p. 479) linked 
survival rates to the departure condition of spring migrants in C.c. 
    In addition to survival, breeding success was suggested by Baker et 
al. (2004, pp. 875, 879) as being linked to food availability in 
Delaware Bay, based on a 47 percent decline in second-year birds 
observed in wintering flocks. However, there may be segregation of 
juvenile and adult red knots on the wintering grounds, and little 
information is available on where juveniles spent the winter months 
(USFWS and Conserve Wildlife Foundation 2012, p. 1). Thus, shifting 
juvenile habitat use cannot be ruled out as a factor in the decline of 
young birds observed at known (adult) wintering areas.
    Although Baker et al. (2004, p. 879) postulated that the observed 
decrease in second-year birds was linked to food availability in 
Delaware Bay, no direct links have been established between horseshoe 
crab egg availability and red knot reproductive success. Red knots 
typically do not rely on stored fat for egg production or the 
subsequent rearing of young, having used up most of those reserves for 
the final migration flight and initial survival on the breeding grounds 
(Morrison 2006, p. 612; Piersma et al. 2005, p. 270; Morrison and 
Hobson 2004, p. 341; Klaassen et al. 2001, p. 794). The fact that body 
stores are not directly used for egg or chick production suggests that 
horseshoe crab egg availability is unlikely to affect red knot 
reproductive rates, other than through an influence on the survival of 
prebreeding adults. However, studies of shorebirds as a group indicate 
that if birds arrive in a poor energetic state on the destination area, 
they would have a very small chance of reproducing successfully 
(Piersma and Baker 2000, p. 123). Further, from studies of the Calidris 
canutus islandica, Morrison (2006, pp. 610-612) and Morrison et al. 
(2005, p. 449) found that a major function of stored fat and protein 
may be to facilitate a transformation from a physiological state 
suitable for migration to one suitable, and possibly required, for 
successful breeding. These findings suggest that a more direct link 
between the condition of red knots leaving Delaware Bay and 
reproductive success could exist but has not yet been documented. 
Modeling for the ARM includes components to test for linkages between 
Delaware Bay departure weights and reproductive success and could 
provide future insights into this question (McGowan et al. 2011b, p. 
Horseshoe Crab--Adaptive Resource Management
    In 2012, the ASMFC adopted the ARM for the management of the 
horseshoe crab population in the Delaware Bay Region (ASMFC 2012e, p. 
1). The ARM was developed with input from shorebird and fisheries 
biologists from the Service, States, and other agencies and 
organizations. The ARM modeling links horseshoe crab and red knot 
populations, to meet the dual objectives of maximizing crab harvest and 
meeting red knot population targets (McGowan et al. 2011b, p. 122). The 
ARM uses competing models to test hypotheses and eventually reduce 
uncertainty about the influence that conditions in Delaware Bay exert 
on red knot populations (McGowan et al. 2011b, pp. 130-131). The 
framework is designed as an iterative process that adapts to new 
information and the success of management actions (ASMFC 2012e, p. 3). 
Under the ARM, the horseshoe crab harvest caps authorized by ASMFC are 
explicitly linked to red knot population recovery targets starting in 
2013 (ASMFC 2012e, p. 4).
    As long as the ARM is in place and functioning as intended, ongoing 
horseshoe crab harvests should not be a threat to the red knot. 
However, the harvest regulations recommended by the ARM require data 
from two annual, baywide monitoring programs--the trawl survey 
conducted by the Virginia Polytechnic Institute (Virginia Tech) and the 
Delaware Bay Shorebird Monitoring Program. No secure funding is in 
place for either of these programs. For example, in fall 2012, the 
trawl survey had to be scaled back due to lack of funds (ASMFC 2012d, 
p. 8). Reduced survey efforts may impact the ability of the ASMFC to 
implement the ARM as intended (ASMFC 2012c, p. 13). If the ARM cannot 
be implemented in any given year, ASMFC would choose between two 
options based on which it determines to be more appropriate--either use 
the previous year's harvest levels (as previously set by the ARM), or 
revert to an earlier management regime (known as Addendum VI, which was 
in effect from August 2010 to February 2012) (ASMFC 2012e, p. 6; ASMFC 
2010, entire). Although the horseshoe crab fishery would continue to be 
managed under either of these options, the explicit link to red knot 
populations would be lost.
    In addition, some uncertainty exists regarding how to define the 
Delaware Bay horseshoe crab population. Currently all crabs harvested 
from New Jersey and Delaware, as well as part of the harvests from 
Maryland and Virginia, are believed to come from the Delaware Bay 
population. This conclusion was based on resightings in these four 
States of crabs that had been marked with tags in Delaware Bay from 
1999 to 2003 (ASMFC 2006, p. 4). Further work (tagging and genetic 
analysis) suggests that little exchange occurs between the Delaware Bay 
and Chesapeake Bay horseshoe crab populations, but crabs do move 
between Delaware Bay and the Atlantic coastal embayments from New 
Jersey through Virginia (ASMFC 2012e, pp. 3-4; Swan 2005, p. 28; Pierce 
et al. 2000, p. 690). However, other information adds complexity to our 
understanding of the population structure. In a genetic analysis of 
horseshoe crabs from Maine to Florida's Gulf coast, King et al. (2005, 
p. 445) found four distinct regional groupings, including a mid-
Atlantic group extending from Massachusetts to South Carolina. In 
addition, in a long-term tagging study, Swan (2005, p. 39) found 
evidence suggesting the existence of subpopulations of Delaware Bay 
horseshoe crabs. Finally, since most tagging efforts, and most 
resightings of tagged crabs, occur on spawning beaches, the 
distribution and movements of horseshoe crabs in offshore waters (where 
most of the harvest occurs via trawls) are poorly known (Swan 2005, pp. 
30, 33, 37). We conclude that the ASMFC's current delineation of the 
Delaware Bay Region horseshoe crab population is based on

[[Page 60071]]

best available information and is appropriate for use in the ARM 
modeling, but we acknowledge some uncertainty regarding the population 
structure and distribution of Delaware Bay horseshoe crabs.
Food Availability--Summary
    Reduced food availability at the Delaware Bay stopover site due to 
commercial harvest of the horseshoe crab is considered a primary causal 
factor in the decline of rufa red knot populations in the 2000s. Due to 
harvest restrictions and other conservation actions, horseshoe crab 
populations showed some signs of recovery in the early 2000s, with 
apparent signs of red knot stabilization (survey counts, rates of 
weight gain) occurring a few years later (as might be expected due to 
biological lag times). Since about 2005, however, horseshoe crab 
population growth has stagnated for unknown reasons. Under the current 
management framework (the ARM), the present horseshoe crab harvest is 
not considered a threat to the red knot. However, it is not yet known 
if the horseshoe crab egg resource will continue to adequately support 
red knot populations over the next 5 to 10 years. In addition, 
implementation of the ARM could be impeded by insufficient funding.
    The causal role of reduced Delaware Bay food supplies in driving 
red knot population declines shows the vulnerability of red knots to 
declines in the quality or quantity of their prey. This vulnerability 
has also been demonstrated in other Calidris canutus subspecies, 
although not to the severe extent experienced by the rufa red knot. In 
addition to the fact that horseshoe crab population growth has 
stagnated, red knots now face several emerging threats to their food 
supplies throughout their nonbreeding range. These threats include 
small prey sizes (from unknown causes) at two key wintering sites on 
Tierra del Fuego, warming water temperatures that may cause mollusk 
population declines and range contractions (including the likely loss 
of a key prey species from the Virginia spring stopover within the next 
decade), ocean acidification to which mollusks are particularly 
vulnerable, physical habitat changes from climate change affecting 
invertebrate communities, possibly increasing rates of mollusk diseases 
due to climate change, invasive marine species from ballast water and 
aquaculture, and the burial and crushing of invertebrate prey from sand 
placement and recreational activities. Although threats to food quality 
and quantity are widespread, red knots in localized areas have shown 
some adaptive capacity to switch prey when the preferred prey species 
became reduced (Escudero et al. 2012, pp. 359, 362; Musmeci et al. 
2011, entire), suggesting some adaptive capacity to cope with this 
threat. Nonetheless, based on the combination of documented past 
impacts and a spectrum of ongoing and emerging threats, we conclude 
that reduced quality and quantity of food supplies is a threat to the 
rufa red knot at the subspecies level, and the threat is likely to 
continue into the future.
Factor E--Asynchronies During the Annual Cycle
    For shorebirds, the timing of arrivals and departures from 
wintering, stopover, and breeding areas must be precise because prey 
abundance at staging areas is cyclical, and there is only a narrow 
window in the arctic summer for courtship and reproduction (Botton et 
al. in Shuster et al. 2003, p. 6). Because the arctic breeding season 
is short, northbound birds must reach the nesting grounds as soon as 
the snow has melted. Early arrival and rapid nesting increases 
reproductive success. However, a countervailing time constraint is that 
the seasonal supply of food resources along the migration pathways 
prevents shorebirds from moving within flight distance of the breeding 
grounds until late spring (Myers et al. 1987, pp. 21-22). The timing of 
southbound migration is also constrained, because the abundance of 
quality prey at stopover sites gradually decreases as the fall season 
progresses (van Gils et al. 2005b, pp. 126-127; Myers et al. 1987, pp. 
21-22). Migration timing is also influenced by the enormous energy 
required for birds to complete the long-distance flights between 
wintering and breeding grounds. Northbound shorebirds migrate in a 
sequence of long-distance flights alternating with periods of intensive 
feeding to restore energy reserves. Most of the energy stores are 
depleted during the next flight; thus, a bird's ability to accumulate a 
small additional energetic reserve may be crucial if its migration gets 
delayed by poor weather or if feeding conditions are poor upon arrival 
at the next destination (Myers et al. 1987, pp. 21-22).
    Particularly for species like the red knot that show fidelity to 
sites with ephemeral food and habitat resources used to fuel long-
distance migration, migrating animals may incur fitness consequences if 
their migration timing and the availability of resources do not 
coincide (i.e., are asynchronous or ``mismatched''). The joint dynamics 
of resource availability and migration timing may play a key role in 
influencing annual shorebird survival and reproduction. The mismatch 
hypothesis is of increasing relevance because of the potential 
asynchronies created by changes in phenology (periodic life-cycle 
events) related to global climate change (McGowan et al. 2011a, p. 2; 
Smith et al. 2011a, p. 575; Meltofte et al. 2007, p. 36).
    Shorebird migration depends primarily on celestial cues (e.g., day 
length) and is, therefore, less influenced by environmental variation 
(e.g., water or air temperatures) than are the life cycles of many of 
their prey species (McGowan et al. 2011a, p. 16); thus, shorebirds are 
vulnerable to worsening asynchronies due to climate change. Studying 
captive Calidris canutus canutus held under a constant temperature and 
light regime for 20 months, Cad[eacute]e et al. (1996, p. 82) found 
evidence for endogenous (caused by factors inside the animal) 
circannual (approximately annual) rhythms of flight feather molt, body 
mass, and plumage molt. Studying C.c. canutus and C.c. islandica, 
Jenni-Eiermann et al. (2002, p. 331) and Landys et al. (2004, p. 665) 
found evidence that thyroid and corticosterone hormones play a role in 
regulating the annual cycles of physical changes.
    We have no evidence concerning the exact nature of the external 
timers that synchronize these endogenous rhythms to the outside world 
(Cad[eacute]e et al. 1996, p. 82). Photoperiod is known to be a 
powerful timer for many species' circannual rhythms, and a role for day 
length as a timer is consistent with observations that captive C.c. 
canutus exposed to day length variation in outdoor aviaries retained 
pronounced annual cycles in molt and body mass; however, these 
experiments do not exclude a role for additional timers besides 
photoperiod. The complex nature of the annual changes in photoperiod 
experienced by trans-equatorial migrants is not fully understood; this 
is especially true for such birds like C. canutus where some 
populations winter in the southern hemisphere while other populations 
winter in the northern hemisphere (Cad[eacute]e et al. 1996, p. 82). 
While uncertainty exists about the extent to which the timing of the 
red knot's annual cycle is controlled by endogenous and celestial 
factors (as opposed to environmental factors); based on the experiments 
with captive C.c. canutus, it is reasonable to conclude that these 
factors will constrain the knot's ability to adapt to the shifting 
temporal and geographic

[[Page 60072]]

patterns of favorable food and weather conditions that are expected to 
occur with global climate change.
    Looking at data from Northern Europe from 1923 to 2008 for 43 
taxonomically diverse birds (including shorebirds but not Calidris 
canutus), Petersen et al. (2012, p. 65) found that short-distance 
migrants arrived an average of 0.38 days earlier per year, while the 
spring arrival of long-distance migrants had advanced an average of 
0.17 days per year. Pooling both groups, spring arrival had shifted an 
average of 3 weeks earlier over the 80-year study period. Changes in 
environmental conditions (e.g., temperature, precipitation) during 
winter and spring explained much of the change in phenology. These 
findings suggest that short-distance migrants may respond more strongly 
to climate change than long-distance migrants, such as the red knot, 
which might adapt more slowly resulting in less time for breeding and 
potentially mis-timed breeding in this group. These results also 
suggest that differential adaptation capacities between short- and 
long-distance migrants could alter the interspecific competition 
pressures faced by various species (Petersen et al. (2012, p. 70) 
caused by the formation of new and novel assemblages of bird species 
that did not previously occur together in space and time.
    The successful annual migration and breeding of red knots is highly 
dependent on the timing of departures and arrivals to coincide with 
favorable food and weather conditions. The frequency and severity of 
asynchronies is likely to increase with climate change. In addition, 
stochastic encounters with unfavorable conditions are more likely to 
result in population-level effects for red knots now than when 
population sizes were larger, as reduced numbers may have reduced the 
resiliency of this subspecies to rebound from impacts.
Asynchronies--Delaware Bay
    Because shorebird staging times are shortest and fueling rates are 
highest at the last stopover site before birds head to the arctic 
breeding grounds, there appears to be little ``slack'' time at late 
stages in the migration (Gonz[aacute]lez et al. 2006, p. 115; Piersma 
et al. 2005, p. 270) (i.e., birds need to arrive and depart within a 
narrow time window and need to attain rapid weight gain during that 
window). For a large majority of red knots, the final stopover before 
the Arctic is in Delaware Bay.
Delaware Bay--Late Arrivals
    Baker et al. (2004, p. 878) found that the late arrival of red 
knots in Delaware Bay was a key synergistic factor (acting in 
conjunction with reduced availability of horseshoe crab eggs) 
accounting for declines in survival rates observed, comparing the 
period 1994 to 1996 with the period 1997 to 2000. These authors noted 
that red knots from southern wintering areas (Argentina and Chile) 
tended to arrive later than northern birds throughout the study period, 
but more so in 2000 and 2001. A large number of knots arrived late 
again in 2002 (Robinson et al. 2003, p. 11). In data from 1998 to 2002, 
Atkinson et al. (2003b, p. 16) found increasing evidence that numbers 
of light-weight birds were passing through the bay between May 20 and 
30. Corroborating evidence comes from Argentina and suggests that, for 
unknown reasons, northward migration of Tierra del Fuego birds had 
become 1 to 2 weeks later since 2000 (Niles et al. 2008, p. 2), which 
probably led to more red knots arriving late in Delaware Bay.
    Research has shown that late-arriving birds have the ability to 
make up lost time by gaining weight at a higher rate than usual, 
provided they have sufficient food resources (Niles et al. 2008, p. 2; 
Atkinson et al. 2007, pp. 885, 889; Robinson et al. 2003, pp. 12-13). 
However, late-arriving birds failed to do so in years (e.g., 2003, 
2005) when horseshoe crab egg availability was low (Niles et al. 2008, 
p. 2; Atkinson et al. 2007, p. 885). Looking at data from 1998 to 2002, 
Atkinson et al. (2003b, p. 16) found that intra-season rates of weight 
gain had not changed significantly. Using an early model linking red 
knot weight gain and subsequent survival, these authors concluded that 
arriving late was actually a more significant factor than food 
availability in the declining percentage of red knots reaching target 
weights by the end of May (Atkinson et al. 2003b, p. 16). In a later 
modeling effort, Atkinson et al. (2007, p. 892) confirmed that fueling 
(temporal patterns and rates of weight gain) proceeded as normal from 
1997 to 1999, from 2001 to 2002, and in 2004, but fueling was below 
normal in 2000, 2003, and 2005 due to poor foraging and weather 
conditions. The results of Atkinson et al. (2007, p. 892) suggest that 
the reduced survival rates calculated by Baker et al. (2004, entire) 
from 1998 to 2002 were more likely the result of late arrivals than 
food availability, since fueling was normal in all but one of those 
    The effects of weather on the red knot's migratory schedule were 
documented in 1999, when a La Ni[ntilde]a event (an occasional abnormal 
cooling of tropical waters in the eastern Pacific from unknown causes) 
occurred and the red knots migrating to Delaware Bay were subject to 
extended, strong headwinds (Robinson et al. 2003, pp. 11-12). The first 
birds arrived almost a week later than normal. Although most red knots 
had left Delaware Bay by the end of May, an unusually large number 
(several thousand) of knots were recorded in central Canada in mid-
June, suggesting that many birds did not reach the breeding grounds or 
quickly returned south without breeding in that year. It is possible 
that many birds did not put on adequate weight as a result of the 
weather-induced delay and were not in a good enough condition to breed 
(Robinson et al. 2003, pp. 11-12). In addition to the unknown causes 
that may have contributed to chronic late arrivals in Delaware Bay in 
the 2000s, stochastic weather events like the 1999 La Ni[ntilde]a can 
affect the timing of the red knot's annual cycle and may become more 
erratic or severe due to climate change.
Delaware Bay--Timing of Horseshoe Crab Spawning
    Even those red knots arriving early or on time in Delaware Bay are 
very likely to face poor feeding conditions if horseshoe crab spawning 
is delayed. Feeding conditions for red knots were poor in those years 
when the timing of the horseshoe crab spawn was out of sync with the 
birds' spring stopover period. In years that spawning was delayed due 
to known weather anomalies (e.g., cold weather, storms), the proportion 
of knots reaching weights of 6.3 oz (180 g) or greater at the end of 
May was very low (e.g., 0 percent in 2003) (Dey et al. 2011a, p. 7; 
Atkinson et al. 2007, p. 892). These observed correlations were 
confirmed by the ARM modeling. The models found strong evidence that 
the timing of horseshoe crab spawning, not simply crab abundance, is 
important to red knot refueling during stopover. If spawning is 
delayed, even with relatively high total crab abundance, the 
probability that a light bird will add enough mass to become a heavy 
bird before departure may be lower (McGowan et al. 2011a, p. 12). The 
timing of horseshoe crab spawning is closely tied to water 
temperatures, and can be delayed by storms. If water temperatures or 
storm patterns in the mid-Atlantic region were to change significantly, 
the timing of spawning could shift and become temporally mismatched 
with shorebird migration (McGowan et al. 2011a, p. 16).

[[Page 60073]]

Horseshoe Crab Spawn--Storms and Weather
    Normal variation in weather is a natural occurrence and is not 
considered a population-level threat to the red knot. However, adverse 
weather events in Delaware Bay can throw off the timing of horseshoe 
crab spawning relative to the red knot's stopover period. Such events 
have the potential to impact a majority of the red knot population, as 
most birds pass through Delaware Bay in spring (Brown et al. 2001, p. 
10). Synergistic effects have also been noted among such weather 
events, habitat conditions, and insufficient horseshoe crab eggs (Dey 
et al. 2011a, p. 7).
    The Delaware Bay stopover period occurs between the typical 
nor'easter (October through April) and hurricane (June through 
November) storm seasons (National Hurricane Center 2012; Frumhoff et 
al. 2007, p. 30). However, late nor'easters do occur in May, such as 
occurred in 2008 when horseshoe crab spawning was delayed and red knot 
feeding conditions were poor. Unusual wind and rain conditions can also 
affect the red knots' distribution among Delaware Bay beaches and 
length of stay, causing variations in their activity and habitat 
selection. High wind and weather events are common in May and in some 
years limit horseshoe crab spawning to creek mouths that are protected 
from rough surf (Dey et al. 2011, pp. 1-2; Clark et al. 1993, p. 702). 
High wave energies transport more eggs in the swash zone (the zone of 
wave action), but these eggs are dispersed or buried, and fewer eggs 
remain on the beach where they are available to shorebirds (Nordstrom 
et al. 2006a, p. 439).
    High wave conditions curtail horseshoe crab spawning (Nordstrom et 
al. 2006a, p. 439). Smith et al. (2011a, pp. 575, 581) found that 
onshore winds that generate waves can delay spawning and create an 
asynchrony for migrating red knots. High levels of food abundance can 
offset some small mismatches in migration timing. Thus, increasing 
abundance of horseshoe crab eggs throughout the stopover period could 
act as a hedge against temporal mismatches between the horseshoe crab 
and shorebird migrations, at least in the near term. Also, select 
beaches with high spawning activity and capacity to retain eggs in 
surface sediments during episodes of high onshore winds could provide a 
reserve of horseshoe crab eggs during the shorebird stopover period, 
even in years when winds cause asynchrony between species migrations 
(Smith et al. 2011a, pp. 575, 581). Therefore, a superabundance of 
horseshoe crab eggs and sufficient high-quality foraging habitats can 
serve to partially offset asynchronies between the red knot stopover 
and the peak of horseshoe crab spawning.
    Future frequency or intensity of storms in Delaware Bay during the 
stopover season may change due to climate change, but predictions about 
future tropical and extra-tropical storm patterns have only ``low to 
medium confidence'' (see supplemental document--Climate Change 
Background). Should storm patterns change, red knots in Delaware Bay 
would be more sensitive to the timing and location of coastal storms 
than to a change in overall frequency. Changes in the patterns of 
tropical or extra-tropical storms that increase the frequency or 
severity of these events in Delaware Bay during May would likely have 
dramatic effects on red knots and their habitats (Kalasz 2008, p. 41) 
(e.g., through direct mortality, delayed horseshoe crab spawning, 
delayed departure for the breeding grounds, and short-term habitat 
Horseshoe Crab Spawn--Water Temperatures
    More certainty is associated with a correlation between the timing 
of horseshoe crab spawning and ocean water temperatures, based on a 
study by Smith and Michels (2006, pp. 487-488). Although horseshoe 
crabs spawn from late spring into early summer, migratory shorebirds 
use Delaware Bay for only a few key weeks in May and early June. In 
some years, horseshoe crab spawning has been early, with a high 
proportion of spawning activity occurring in May, and therefore better 
synchronized with the shorebird stopover period. In other years 
spawning has been late, with a low proportion of spawning in May, 
resulting in poor shorebird feeding conditions during the stopover 
period. Average daily water temperature has been statistically 
correlated with the percent of spawning that takes place in May, though 
the relationship is stronger in New Jersey than in Delaware. In the 
years with the lowest May spawning percentages, average water 
temperatures did not exceed 57.2 [deg]F (14 [deg]C) during May, and 
daily water temperatures were not consistently above 59 [deg]F (15 
[deg]C) until late May. In the other years, daily water temperatures 
were consistently above 59 [deg]F (15 [deg]C) by mid-May (Smith and 
Michels 2006, pp. 487-488). After adjusting for the day of the first 
spring tide, the day of first spawning has been 4 days earlier for 
every 1.8 [deg]F (1 [deg]C) rise in mean daily water temperature in May 
(Smith et al. 2010b, p. 563).
    Climate change does not necessarily mean a linear increase in 
temperatures and an amelioration of winters in the mid-Atlantic region. 
As the climate changes, we could see both extremes of weather from year 
to year, with some years being warmer and others being colder. The 
colder years could cause horseshoe crab spawning to be delayed past the 
shorebird stopover period (Kalasz 2008, p. 41). In addition, impacts to 
red knots from increasingly extreme precipitation events (see 
supplemental document--Climate Change Background) are not known, but 
may include temporary water temperature changes that could affect the 
timing of horseshoe crab spawning activity.
    Conversely, average air and water temperatures are expected to 
continue rising. In the Northeast, annual average air temperature has 
increased by 2 [deg]F (1.1 [deg]C) since 1970, with winter temperatures 
rising twice as much (USGCRP 2009, p. 107). Over the next several 
decades, temperatures in the Northeast are projected to rise an 
additional 2.5 to 4 [deg]F (1.4 to 2.2 [deg]C) in winter and 1.5 to 3.5 
[deg]F (0.8 to 1.9 [deg]C) in summer (USGCRP 2009, p. 107). Coastal 
waters are ``very likely'' to continue to warm by as much 4 to 8 [deg]F 
(2.2 to 4.4 [deg]C) in this century, both in summer and winter (USGCRP 
2009, p. 151). Spring migrating red knots could benefit if warming 
ocean temperatures result in fewer years of delayed horseshoe crab 
spawning. However, earlier spawning could exacerbate the problems faced 
by late-arriving knots that already struggle to gain sufficient weight. 
Under extreme warming, the timing of peak spawning could theoretically 
even shift earlier than the peak red knot stopover season. Using the 
findings of Smith et al. (2010b, entire), spawning could shift nearly 9 
to 18 days earlier with water temperature increases of 4 to 8 [deg]F 
(2.2 to 4.4 [deg]C).
Asynchronies--Other Spring Stopover Areas
    Outside of Delaware Bay, migrating red knots feed primarily on 
bivalves and other mollusks. Spring migrating knots seem to follow a 
northward ``wave'' in prey quality (i.e., flesh-to-shell ratios); 
research suggests that the birds locate and time their stopovers to 
coincide with local peaks in prey quality, which occur during the 
reproductive seasons of intertidal invertebrates (van Gils et al. 
2005a, p. 2615) when normally hard-shelled bivalves (i.e., difficult to 
digest especially given the birds' physiological digestive changes) are 
made available to knots through spat or juveniles with thinner shells. 
Based on a long-term

[[Page 60074]]

data set (1973 to 2001) from the western Wadden Sea, Philippart et al. 
(2003, p. 2171) found that population dynamics of common intertidal 
bivalves are strongly related to seawater temperatures, and rising 
seawater temperatures affect recruitment by decreasing reproductive 
output and advancing the timing of bivalve spawning in spring. Thus, 
red knots are vulnerable to changes in the reproductive timing and the 
geographic ranges of their prey, such as could be precipitated by 
climate change (see examples of blue mussel spat in Virginia and 
horseshoe crab eggs in Delaware Bay discussed above).
    Based on observations from 1998 to 2003, Gonz[aacute]lez et al. 
(2006, p. 109) found that an early March departure date of red knots 
from San Antonio Oeste, Argentina, generally corresponded to an early 
arrival date in Delaware Bay. The early migrating birds exhibited a 
higher return rate in later years, suggesting higher survival rates for 
red knots that arrive earlier in Delaware Bay. These findings are 
consistent with observation from Delaware Bay that an increasing number 
of late-arriving knots, along with reduced horseshoe crab egg 
availability, were both tied to lower survival rates observed in the 
early 2000s (Niles et al. 2008, p. 2; Baker et al. 2004, p. 878).
    At Fracasso Beach on Pen[iacute]nsula Vald[eacute]s, Argentina, 
Hern[aacute]ndez (2009, p. 208) found a significant correlation during 
March and April between the presence of shorebirds and the biomass of 
the clam Darina solenoids, suggesting that the occurrence of shorebirds 
at this site must depend largely on the available food supply. Analysis 
of weekly counts at Fracasso Beach during March and April from 1994 to 
2005 showed some trends in the phenology of the migration of red knots. 
Generally, from 1994 to 1999, red knots occurred during both March and 
April, but in 2000 practically none arrived in March. Moreover, in 2004 
and 2005, the first red knots were not recorded until May. 
Hern[aacute]ndez (2009, p. 208) concluded that this delayed stopover at 
Pen[iacute]nsula Vald[eacute]s was reflected in similar changes at 
other sites along the West Atlantic Flyway (e.g., San Antonio Oeste, 
Delaware Bay), but the cause is unknown.
    After 2000, increasing proportions of birds arrived late and with 
low weights at stopover sites in South and North America, suggesting 
that red knots face additional problems somewhere en route. Indeed, 
observations from a key Tierra del Fuego wintering area (R[iacute]o 
Grande) in 1995, 2000, and 2008 indicated that wintering conditions at 
this site had deteriorated, as energy intake rates dropped sharply due 
to smaller prey sizes and human disturbance (Escudero et al. 2012, p. 
362). Escudero et al. (2012, p. 362) suggested declining foraging 
conditions at R[iacute]o Grande might offer at least a partial 
explanation for red knots after 2000 arriving late, and with low 
weights at stopover sites in South and North America.
    We have no information to explain why the spring migration of some 
red knots wintering in Argentina and Chile apparently shifted later in 
the mid-2000s, exacerbating the population effects from reduced 
horseshoe crab egg supplies in Delaware Bay. Escudero et al. (2012, p. 
362) suggested that problems in one wintering area may be a factor, but 
the full explanation is unknown. Regardless of the cause, if the trend 
of later spring migrations continues, it may exacerbate emerging 
asynchronies with mollusk prey at other stopover areas, since the 
reproductive window of bivalves and other species is likely to shift 
earlier in response to warming water temperatures (Philippart et al. 
2003, p. 2171).
    However, red knots may show at least some adaptive capacity in 
their migration strategies. For example, from 2000 to 2003, a study of 
a Tierra del Fuego wintering area (R[iacute]o Grande) and the first 
major South American stopover site (San Antonio Oeste) found that red 
knots took a direct northward flight between the two areas in 2000 and 
2001. However, in 2002, birds stopped to feed in intermediate wetlands, 
leaving R[iacute]o Grande earlier but arriving later in San Antonio 
Oeste. In 2003, both early and late patterns were observed. Red knots 
arriving early at San Antonio Oeste also arrived significantly earlier 
in Delaware Bay (Gonz[aacute]lez et al. in International Wader Study 
Group 2003 p. 18). These findings, and those of Gonz[aacute]lez et al. 
(2006, p. 115), show some diversity and flexibility of the red knot 
migration strategies. These characteristics may be an advantage in 
helping red knots adapt to temporal changes in resource availability 
along the flyway.
Asynchronies--Fall Migration
    Preliminary results of efforts to track red knot migration routes 
using geolocators found that two of three birds likely detoured from 
normal migration paths to avoid adverse weather during the fall 
migration (Niles et al. 2010a, p. 129). These birds travelled an extra 
640 to 870 mi (1,030 to 1,400 km) to avoid storms. The extra flying 
represents substantial additional energy expenditure, which on some 
occasions may lead to mortality (Niles et al. 2010a, p. 129). The 
timing of fall migration coincides with hurricane season. As discussed 
in the supplemental document ``Climate Change Background,'' increasing 
hurricane intensity is ongoing and expected to continue. Hurricane 
frequency is not expected to increase globally in the future, but may 
have increased in the North Atlantic over recent decades. However, 
predictions about changing storm patterns are associated with ``low'' 
to ``medium'' confidence levels (IPCC 2012, p. 13). Therefore, we are 
uncertain how or to what extent red knots will be affected by changing 
storm patterns during fall migration.
    Red knots may also face asynchronies with the periods of peak prey 
abundance in fall, similar to those discussed above for the spring 
migration. Studying Calidris canutus islandica in the Dutch Wadden Sea, 
van Gils et al. (2005b, pp. 126-127) found that gizzards are smallest 
just following the breeding season because while in the Arctic the 
birds feed on soft-bodied arthropods. Upon arrival at the fall staging 
area, gizzards enlarge to their normal nonbreeding size. During their 
`small-gizzard' phase the birds rely heavily on high-quality prey 
(e.g., high flesh-to-shell ratios), which are most abundant early in 
the stopover period when most birds arrive. Birds that arrive late at 
the staging area might struggle to keep their energy budgets balanced, 
let alone refuel to gain mass and continue on to the wintering grounds. 
This work by van Gils et al. (2005b, pp. 126-127) shows the importance 
of timing to food availability during fall migration in C. canutus. The 
timing of fall migration in shorebirds including red knots is also 
important to avoid the peak migration of avian predators (see Factor C 
above) (L. Niles pers. comm. November 19, 2012; Meltofte et al. 2007, 
p. 27; Lank et al. 2003, p. 303).
Asynchronies--Breeding Grounds
    As explained previously, the northbound red knot migration is time-
constricted. Birds must arrive on arctic breeding grounds at the right 
time and with sufficient remaining energy and nutrient stores. In 
fitness terms, everything else in the annual cycle may be subservient 
to arrival timing. Knots need to reach the Arctic just as snow is 
melting, lay their eggs, and hatch them in time for the insect 
emergence (Piersma et al. 2005, p. 270; Clark in Farrell and Martin 
1997, p. 23). Insects are the primary food source for red knot chicks, 
and for adults during the breeding season. Modeling results from the 
ARM suggest that indices of arctic conditions are predictors of the 

[[Page 60075]]

survival probability of adult red knots, and have stronger effects on 
survival than departure weights from Delaware Bay (McGowan et al. 
2011a, p. 13).
    Adverse weather in the Arctic can cause years with little to no 
productivity for shorebird species. Conditions for breeding are highly 
variable among sites and regions. The factors most affected by annual 
variation in weather include whether to breed upon arrival on the 
breeding grounds, the timing of egg-laying, and the chick growth period 
(Meltofte et al. 2007, p. 7). In much of the Arctic, initiation dates 
of clutches (the group of eggs laid by one female) are highly 
correlated with snowmelt dates. In regions and years where extensive 
snowmelt occurs before or soon after shorebird arrival, the decision to 
breed and clutch initiation dates both appear to be a function of food 
availability for females. Once incubation is initiated, adult 
shorebirds appear fairly resilient to variations in temperature, with 
nest abandonment generally limited to cases of severe weather when new 
snow covers the ground. Feeding conditions for chicks are highly 
influenced by weather, affecting juvenile production (Meltofte et al. 
2007, p. 7). For a number of shorebird species, productivity has been 
correlated with climate variables known to affect nesting (in June) or 
brood-rearing (in July) success in a positive (temperature) or negative 
(snow depth, wind, precipitation) manner (Meltofte et al. 2007, p. 25).
    Anticipated climate changes are expected to be particularly 
pronounced in the Arctic, and extensive and dramatic changes in snow 
and weather regimes are predicted for most tundra areas (Meltofte et 
al. 2007, p. 11) where red knots breed. (See Factor A--Breeding Habitat 
Loss from Warming Arctic Conditions, above, for recent rates and 
predictions of arctic warming and the eco-regional classification of 
the red knot's current breeding range.) However, forecasting the 
effects of changing arctic weather patterns on shorebirds is associated 
with high uncertainty. Under late 20th century climate conditions, 
studies have found that shorebird reproductive success is closely tied 
to weather and temperature during the breeding season. However, these 
findings may tell us little about the effects of climate variables on 
reproductive rates in the future, over a longer time scale, and with a 
much larger amplitude of climate change. Although arctic shorebirds are 
resilient to great interannual variability, we do not know to what 
extent the birds are able to adapt to the long-term and fast-changing 
climatic conditions that are predicted to occur in coming decades 
(Meltofte et al. 2007, p. 34).
Breeding Grounds--Insect Prey
    Schekkerman et al. (2003, p. 340) found that growth rates of 
Calidris canutus chicks were strongly correlated with weather-induced 
and seasonal variation in the availability of invertebrate prey within 
arctic nesting habitats, underscoring the importance of timing of 
reproduction so that chicks can make full use of the summer peak in 
insect abundance. During studies of C. canutus islandica at a nesting 
area in eastern Canada, both adults and juveniles were found to put on 
large amounts of fat prior to migration, suggesting that they make a 
long-haul flight out of the Arctic to the first fall stopover site. The 
period of peak arthropod availability is not only during the peak chick 
rearing season, but also when many adult shorebirds (principally 
females that have abandoned broods to the care of the male) are 
actively accumulating fat and other body stores before departure from 
the Arctic (Meltofte et al. 2007, p. 24).
    Tulp and Schekkerman (2008, p. 48) developed models of the 
relationship between weather and arthropod (i.e., insect) abundance 
based on 4 recent years, then used the models to project insect 
abundance backwards in time (``hindcast'') based on weather records 
over a 30-year period. The hindcasted dates of peak arthropod abundance 
advanced during the study period, occurring 7 days earlier in 2003 than 
in 1973. The timing of the period during which shorebirds have a 
reasonable probability of finding enough food to grow has also changed, 
with the highest probabilities now occurring at earlier dates than in 
the past. At the same time, the overall length of the period with 
probabilities of finding enough food has remained unchanged (e.g., same 
number of days of availability, only sooner). The result is an 
advancement of the optimal breeding date for breeding birds. To take 
advantage of the new optimal breeding time, arctic shorebirds must 
advance the start of breeding, and this change could affect the entire 
migration schedule (Tulp and Schekkerman 2008, p. 48). If such a change 
is beyond the adaptive capacity of red knots, this species will likely 
face increasing asynchronies with its insect prey during the breeding 
season, thereby affecting reproductive output. The potential uncoupling 
of phenology of food resources and breeding events is a major concern 
for the red knot (COSEWIC 2007, p. 40).
    Even when insect abundance is high, energy budgets of breeding red 
knots may be tight due to high energy expenditure levels. During the 
incubation phase in the High Arctic, tundra-breeding shorebirds appear 
to incur among the highest daily energy expenditure levels of any time 
of the year (Piersma et al. 2003b, p. 356). The rates of energy 
expenditure measured in this region are among the highest reported in 
the literature, reaching inferred ceilings of sustainable energy 
turnover rates (Piersma et al. 2003b, p. 356). If decreased prey 
abundance requires birds to spend more time foraging, adverse effects 
to the energy budget would be further exacerbated, possibly impacting 
survival rates because red knots foraging away from the nest on open 
tundra expend almost twice as much energy as during nest incubation 
(Piersma et al. 2003b, p. 356).
    Although not yet documented for red knots, the links between 
temperature, prey, and reproductive success have been established in 
other northern-nesting shorebirds. In one sub-Arctic-breeding shorebird 
species, Pearce-Higgens et al. (2010, p. 12) linked population changes 
to previous August temperatures through the effect of temperature on 
the abundance of the species' insect prey. Predictions of annual 
productivity, based on temperature-mediated reductions in prey 
abundance, closely match observed bird population trends, and 
forecasted warming indicates significant likelihood of northward range 
contraction (e.g., local extinction) (Pearce-Higgens et al. 2010, p. 
    The best available scientific data indicate that red knots will 
likely be negatively affected by increased asynchronies between the 
breeding season and the window of optimal insect abundance. However, we 
are uncertain how or to what extent red knots may be able to adapt 
their annual cycle, geographic range, or breeding strategy to cope with 
these predicted ecosystem changes in the Arctic.
Breeding Grounds--Snowmelt
    Field studies from several breeding sites have shown the 
sensitivity of red knots to the date of snow melt. At 4 sites in the 
eastern Canadian Arctic, Smith et al. (2010a, p. 292) monitored the 
arrival of 12 species (including red knot) and found 821 nests over 11 
years. Weather was highly variable over the course of the study, and 
the date of 50 percent snow cover varied by up to 3 weeks among years. 
In contrast, timing of bird arrival varied by 1 week or less at the 
sites and was not well predicted by local conditions such as 
temperature, wind, or snow melt. Timing of breeding was related to the 
date of 50 percent

[[Page 60076]]

snow melt, with later snow melt resulting in delayed breeding (Smith et 
al. 2010a, p. 292). These findings suggest that the suite of cues that 
control the timing of shorebird arrival in the Arctic are not equipped 
to adjust for annual weather variations that take place on the breeding 
    In 1999, Morrison et al. (2005, p. 455) found that post-arrival 
body masses of Calidris canutus islandica at a breeding site on 
Ellesmere Island, Canada, were lower than the long-term mean. Many 
shorebirds were unable to breed, or bred late, due to extensive early-
season (June) snow cover. The need to use stored energy reserves for 
survival or supplementing lower than usual local food resources in that 
year may have contributed to delayed or failed breeding (Morrison et 
al. 2005, p. 455). At a site on Southampton Island in Canada, late 
snowmelt and adverse weather conditions, combined with predation, 
contributed to poor productivity in 2004, and may have also 
significantly increased mortality of adult red knots. Canadian 
researchers reported that most Arctic-breeding birds failed to breed 
successfully in 2004 (Niles et al. 2005, p. 4).
    Trends toward earlier snowmelt dates have been documented in North 
America in recent years (IPCC 2007b, p. 891). Earlier snowmelts in the 
Arctic from 2020 to 2080 are ``very likely'' (ACIA 2005, p. 470). As 
years of late snowmelt have typically had an adverse effect on 
shorebird breeding, reduced frequency of late-melt years may have a 
short-term benefit to red knots. Warming trends may benefit arctic 
shorebirds in the short term by increasing both survival and 
productivity (Meltofte et al. 2007, p. 7). However, it is unknown how 
red knots would be affected if snowmelts become substantially earlier 
than the start of the breeding season (see Ims and Fuglei 2005 for 
consideration of the complex ways tundra ecosystems may respond to 
climate change).
Breeding Grounds--Snow Depth
    Modeling for the ARM suggested that higher snow depth in the 
breeding grounds on June 10 (about 7 days after peak arrival of red 
knots) has a strong positive influence on red knot survival 
probability, regardless of the birds' weights upon departure from 
Delaware Bay (McGowan et al. 2011a, p. 13). In contrast, several 
studies to date have found a negative effect of snow cover on breeding 
success (McGowan et al. 2011a, p. 13; Meltofte et al. 2007, p. 25). 
These seemingly contradictory findings have many possible explanations: 
Birds may skip breeding in years with heavy snow after arriving in the 
Arctic and survive at higher rates without the physiological stresses 
of breeding; snow may determine annual moisture and water in the 
environment and thereby drive the production of insect prey; red knot 
survival may be tied to lemming cycles, which are in turn closely 
linked to snow depth; or the selected weather stations may not be 
representative of mean snow depth throughout the red knot's breeding 
range (McGowan et al. 2011a, p. 13). Regardless of the explanation, if 
this strong linkage between snow depth and survival proves correct, 
arctic warming trends that reduce snow depths would adversely affect 
red knot survival rates. Such an impact could negate the potential 
benefits of increased productivity from earlier snowmelt.
    The red knot's life history strategy makes this species inherently 
vulnerable to mismatches in timing between its annual cycle and those 
periods of optimal food and weather conditions upon which it depends. 
For unknown reasons, more red knots arrived late in Delaware Bay in the 
early 2000s, which is generally accepted as a key causative factor 
(along with reduced supplies of horseshoe crab eggs) behind red knot 
population declines that were observed over this same timeframe. Thus, 
the red knot's sensitivity to timing asynchronies has been demonstrated 
through a population-level response. Both adequate supplies of 
horseshoe crab eggs and high-quality foraging habitat in Delaware Bay 
can serve to partially mitigate minor asynchronies at this key stopover 
site. However, the factors that caused delays in the spring migrations 
of red knots from Argentina and Chile are still unknown, and we have no 
information to indicate if this delay will reverse, persist, or 
    Superimposed on this existing threat of late arrivals in Delaware 
Bay are new threats of asynchronies emerging due to climate change. 
Climate change is likely to affect the reproductive timing of horseshoe 
crabs in Delaware Bay, mollusk prey species at other stopover sites, or 
both, possibly pushing the peak seasonal availability of food outside 
of the windows when red knots rely on them. In addition, both field 
studies and modeling have shown strong links between the red knot's 
reproductive output and conditions in the Arctic including insect 
abundance and snow cover. Climate change may also cause shifts in the 
period of optimal arctic conditions relative to the time period when 
red knots currently breed.
    The red knot's adaptive capacity to deal with numerous changes in 
the timing of resource availability across its geographic range is 
largely unknown. A few examples suggest some flexibility in migration 
strategies. However, available information suggests that the timing of 
the red knot's annual cycle is controlled at least partly by celestial 
and endogenous cues, while the reproductive seasons of prey species, 
including horseshoe crabs and mollusks, are largely driven by 
environmental cues such as water temperature. These differences between 
the timing cues of red knots and their prey suggest limitations on the 
adaptive capacity of red knots to deal with numerous changes in the 
timing of resource availability across their geographic range.
    Based on the combination of documented past impacts and a spectrum 
of ongoing and emerging threats, we conclude that asynchronies 
(mismatches between the timing of the red knot's annual cycles and the 
periods of favorable food and weather upon which it depends) are likely 
to cause deleterious subspecies-level effects.
Factor E--Human Disturbance
    In some wintering and stopover areas, red knots and recreational 
users (e.g., pedestrians, ORVs, dog walkers, boaters) are concentrated 
on the same beaches (Niles et al. 2008, pp. 105-107; Tarr 2008, p. 
134). Recreational activities affect red knots both directly and 
indirectly. These activities can cause habitat damage (Schlacher and 
Thompson 2008, p. 234; Anders and Leatherman 1987, p. 183), cause 
shorebirds to abandon otherwise preferred habitats, negatively affect 
the birds' energy balances, and reduce the amount of available prey 
(see Reduced Food Availability, above). Effects to red knots from 
vehicle and pedestrian disturbance can also occur during construction 
of shoreline stabilization projects including beach nourishment. Red 
knots can also be disturbed by motorized and nonmotorized boats, 
fishing, kite surfing, aircraft, and research activities (K. Kalasz 
pers. comm. November 17, 2011; Niles et al. 2008, p. 106; Peters and 
Otis, 2007, p. 196; Harrington 2005b, pp. 14-15; 19-21; Meyer et al. 
1999, p. 17; Burger 1986, p. 124) and by beach raking (also called 
grooming or cleaning, see Factor A above). In Delaware Bay, red knots 
could also potentially be disturbed by hand-harvest of horseshoe crabs 
(see Reduced Food Availability, above) during the spring migration 
stopover period, but under the current management of this fishery State 

[[Page 60077]]

from New Jersey to coastal Virginia are closed to horseshoe crab 
harvest and landing from January 1 to June 7 each year (ASMFC 2012a, p. 
4); thus, disturbance from horseshoe crab harvest is no longer 
occurring. Active management can be effective at reducing and 
minimizing the adverse effects of recreational disturbance (Burger and 
Niles in press, entire; Forys 2011, entire; Burger et al. 2004, 
entire), but such management is not occurring throughout the red knot's 
Disturbance--Timing and Extent
    Although the timing, frequency, and duration of human and dog 
presence throughout the red knot's U.S. range are not fully known, 
periods of recreational use tend to coincide with the knot's spring and 
fall migration periods (WHSRN 2012; Maddock et al. 2009, entire; 
Mizrahi 2002, p. 2; Johnson and Baldassarre 1988, p. 220; Burger 1986, 
p. 124). Burger (1986, p. 128) found that red knots and other 
shorebirds at two sites in New Jersey reacted more strongly to 
disturbance (i.e., flew away from the beach where they were foraging or 
roosting) during peak migration periods (May and August) than in other 
    Human disturbance within otherwise suitable red knot migration and 
winter foraging or roosting areas was reported by biologists as 
negatively affecting red knots in Massachusetts, Virginia, North 
Carolina, South Carolina, Georgia, and Florida (USFWS 2011b, p. 29). 
Some disturbance issues also remain in New Jersey (both Delaware Bay 
and the Atlantic coast) despite ongoing, and largely successful, 
management efforts since 2003 (NJDEP 2013; USFWS 2011b, p. 29; Niles et 
al. 2008, pp. 105-106). Delaware also has a management program in place 
to limit disturbance (Kalasz 2008, pp. 36-38). In Florida, the most 
immediate and tangible threat to migrating and wintering red knots is 
apparently chronic disturbance (Niles et al. 2008, p. 106; Niles et al. 
2006, entire), which may be affecting the ability of birds to maintain 
adequate weights in some areas (Niles 2009, p. 8).
    In many areas, migration and wintering habitat for the piping 
plover overlaps considerably with red knot habitats. Because the two 
species use similar habitats in the Southeast, and both are documented 
to be affected by disturbance, we can infer the extent of potential 
human disturbance to red knots from piping plover data in this region. 
Based on a preliminary review of disturbance in piping plover wintering 
habitats from North Carolina to Texas, pedestrians and dogs are 
widespread on beaches in this region (USFWS 2009, p. 46). LeDee et al. 
(2010, pp. 343-344) surveyed land managers of designated wintering 
piping plover critical habitat sites across seven southern States and 
documented the extent of beach access and recreation. All but 4 of the 
43 reporting sites owned or managed by Federal, State, and local 
governmental agencies or by nongovernmental organizations allowed 
public beach access year-round (88 percent of the sites). At the sites 
allowing public access, 62 percent of site managers reported more than 
10,000 visitors from September to March, and 31 percent reported more 
than 100,000 visitors in this period. However, more than 80 percent of 
the sites allowing public access did not allow vehicles on the beach, 
and half did not allow dogs during the winter season (as cited in USFWS 
2012a, p. 35).
    Disturbance of red knots has also been reported from Canada. In the 
Province of Quebec, specifically on the Magdalen Islands, feeding and 
resting red knots are frequently disturbed by human activities such as 
clam harvesting and farming, kite surfing, and seal rookery observation 
(USFWS 2011b, p. 29). With the increasing popularity of ecotourism, 
more visitors from around the world come to the shores of the Bay of 
Fundy in Canada, but existing infrastructure is insufficient to 
minimize disturbance to roosting shorebirds during high-tide periods. 
In addition, access to the shoreline is increasing due to ORV use 
(WHSRN 2012).
    Areas of South America also have documented red knot disturbance. 
In Tierra del Fuego, wintering red knots are often disturbed around 
R[iacute]o Grande City, Argentina, by ORVs, motorcycles, walkers, 
runners, fishermen, and dogs (Niles et al. 2008, p. 107; COSEWIC 2007, 
p. 36). The City of R[iacute]o Grande has recently grown extensively 
towards the sea and river margins. Escudero et al. (2012, p. 358) 
reported that pedestrians, ORVs, and unleashed dogs on the gravel beach 
during high tide caused red knots to fly from one spot to another or to 
move farther away from feeding areas. During outgoing tides, as prime 
intertidal foraging habitats became exposed, red knots were disturbed 
and were flushed continuously by walkers, ORVs, and dogs (Escudero et 
al. 2012, p. 358).
    In Patagonian Argentina, disturbance of migrating red knots has 
been reported from shorebird reserve areas at R[iacute]o Gallegos, 
Pen[iacute]nsula Vald[eacute]s, Bah[iacute]a San Antonio (San Antonio 
Oeste), and Bah[iacute]a Samboromb[oacute]n (WHSRN 2012; Niles et al. 
2008, p. 107). Coastal urban growth at R[iacute]o Gallegos has 
increased disturbances to shorebirds, especially during high tide when 
they gather in a limited number of spots very close to shore. Dogs and 
people frequently interrupt the birds' resting and feeding activities. 
Various recreational activities, including boating, sport fishing, 
hiking, and dog walking, take place at urban sites near the coast and 
on the periphery of the city. These seasonal activities are 
concentrated in the austral spring and summer (WHSRN 2012), when red 
knots are present.
    Both shorebirds and people are attracted to the pristine beaches in 
Bah[iacute]a San Antonio, Argentina. For example, Las Grutas Beach 
draws 300,000 tourists every summer, a number that has increased 20 
percent per year over the past decade, and the timing of which 
corresponds with the red knot's wintering use. New access points, 
buildings, and tourist amusement facilities are being constructed along 
the beach. Lack of planning for this rapid expansion has resulted in 
uncontrolled tourist disturbance of crucial roosting and feeding areas 
for migratory shorebirds, including red knots (WHSRN 2012).
    Management efforts have begun to mitigate disturbance at some South 
American sites. Campaigns to build alternative ORV trails away from 
shorebird areas, and to raise public awareness, have helped reduce 
disturbance in Tierra del Fuego, R[iacute]o Gallegos, and Bah[iacute]a 
San Antonio (American Bird Conservancy 2012a, p. 5). The impact of 
human disturbance was successfully controlled at roosting and feeding 
sites at Los Alamos near Las Grutas (Bah[iacute]a San Antonio) by 
``environmental rangers'' charged with protecting shorebird roosting 
sites and providing environmental education (WHSRN 2012). However, 
other key shorebird sites do not yet have any protection.
Disturbance--Precluded Use of Preferred Habitats
    Where shorebirds are habitually disturbed, they may be pushed out 
of otherwise preferred roosting and foraging habitats (Colwell et al. 
2003, p. 492; Lafferty 2001a, p. 322; Lu[iacute]s et al. 2001, p. 72; 
Burton et al. 1996, pp. 193, 197-200; Burger et al. 1995, p. 62). 
Roosting knots are particularly vulnerable to disturbance because birds 
tend to concentrate in a few small areas during high tides, and 
availability of suitable roosting habitats is already constrained by 
predation pressures and energetic costs such as traveling between 
roosting and foraging areas (L. Niles pers. comm. November 19, 2012; 
Rogers et al. 2006a, p. 563; Colwell et al. 2003, p. 491; Rogers 2003, 
p. 74).

[[Page 60078]]

    Exclusion of shorebirds from preferred habitats due to disturbance 
has been noted throughout the red knot's nonbreeding range. For 
example, Pfister et al. (1992, p. 115) found sharper declines in red 
knot abundance at a disturbed site in Massachusetts than at comparable 
but less disturbed areas. On the Atlantic coast of New Jersey, findings 
by Mizrahi (2002, p. 2) generally suggest a negative relationship 
between human and shorebird densities; specifically, sites that allowed 
swimming had the greatest densities of people and the fewest 
shorebirds. At two sites on the Atlantic coast of New Jersey, Burger 
and Niles (in press) found that disturbed shorebird flocks often did 
not return to the same place or even general location along the beach 
once they were disturbed, with return rates at one site of only eight 
percent for monospecific red knot flocks. In Delaware Bay, Karpanty et 
al. (2006, p. 1707) found that potential disturbance reduced the 
probability of finding red knots on a given beach, although the effect 
of disturbance was secondary to the influence of prey resources. In 
Florida, sanderlings seemed to concentrate where there were the fewest 
people (Burger and Gochfeld 1991, p. 263). From 1979 to 2007, the mean 
abundance of red knots on Mustang Island, Texas decreased 54 percent, 
while the mean number of people on the beach increased fivefold (Foster 
et al. 2009, p. 1079). In 2008, Escudero et al. (2012, p. 358) found 
that human disturbance pushed red knots off prime foraging areas near 
R[iacute]o Grande in Argentinean Tierra del Fuego, and that disturbance 
was the main factor affecting roost site selection.
    Although not specific to red knot, Forgues (2010, p. ii) found the 
abundance of shorebirds declined with increased ORV frequency, as did 
the number and size of roosts. Study sites with high ORV activity and 
relatively high invertebrate abundance suggest that shorebirds may be 
excluded from prime food sources due to disturbance from ORV activity 
itself (Forgues 2010, p. 7). Tarr (2008, p. 133) found that disturbance 
from ORVs decreased shorebird abundance and altered shorebird habitat 
use. In experimental plots, shorebirds decreased their use of the wet 
sand microhabitat and increased their use of the swash zone in response 
to vehicle disturbance (Tarr 2008, p. 144).
Disturbance--Effects to Energy Budgets
    Disturbance of shorebirds can cause behavioral changes resulting in 
less time roosting or foraging, shifts in feeding times, decreased food 
intake, and more time and energy spent in alert postures or fleeing 
from disturbances (Defeo et al. 2009, p. 3; Tarr 2008, pp. 12, 134; 
Burger et al. 2007; p. 1164; Thomas et al. 2003, p. 67; Lafferty 2001a, 
p. 315; Lafferty 2001b, p. 1949; Elliott and Teas 1996, pp. 6-9; Burger 
1994, p. 695; Burger 1991, p. 39; Johnson and Baldassarre 1988, p. 
220). By reducing time spent foraging and increasing energy spent 
fleeing, disturbance may hinder red knots' ability to recuperate from 
migratory flights, maintain adequate weights, or build fat reserves for 
the next phase of the annual cycle (Clark in Farrell and Martin 1997, 
p. 24; Burger et al. 1995, p. 62). In addition, stress such as frequent 
disturbance can cause red knots to stop molting before the process is 
complete (Niles 2010b), which could potentially interfere with the 
birds' completion of the next phase of their annual cycle.
    Although population-level impacts cannot be concluded from species' 
differing behavioral responses to disturbance (Stillman et al. 2007; p. 
73; Gill et al. 2001, p. 265), behavior-based models can be used to 
relate the number and magnitude of human disturbances to impacts on the 
fitness of individual birds (Goss-Custard et al. 2006, p. 88; West et 
al. 2002, p. 319). When the time and energy costs arising from 
disturbance were included, modeling by West et al. (2002, p. 319) 
showed that disturbance could be more damaging than permanent habitat 
loss. Modeling by Goss-Custard et al. (2006, p. 88) was used to 
establish critical thresholds for the frequency with which shorebirds 
can be disturbed before they die of starvation. Birds can tolerate more 
disturbance before their fitness levels are reduced when feeding 
conditions are favorable (e.g., abundant prey, mild weather) (Niles et 
al. 2008, p. 105; Goss-Custard et al. 2006, p. 88).
    At one California beach, Lafferty (2001b, p. 1949) found that more 
than 70 percent of birds flew when disturbed, and species that forage 
lower on the beach were disproportionally affected by disturbance 
because contact with people was more frequent. This finding would apply 
to red knots, as they forage in the intertidal zone. At two Atlantic 
coast sites in New Jersey, Burger and Niles (in press) found that 70 
percent of shorebird flocks with red knots flew when disturbed, whether 
the flocks were monospecific or contained other species as well. In two 
New Jersey bays, Burger (1986, p. 125) found that 70 percent of 
shorebirds, including red knots, flew when disturbed, including 25 
(Raritan Bay) to 48 (Delaware Bay) percent that flew away and did not 
return. Birds in smaller flocks tended to be more easily disturbed than 
those in larger flocks. Explanatory variables for differences in 
response rate included date, duration of disturbance, distance between 
the disturbance and the birds, and the number of people involved in the 
disturbance (Burger 1986, pp. 126-127). On some Delaware Bay beaches, 
the percent of shorebirds that flew away and did not return in response 
to disturbance increased between 1982 and 2002 (Burger et al. 2004, p. 
    In Florida, sanderlings ran or flew to new spots when people moved 
rapidly toward them, or when large groups moved along the beach no 
matter how slow the movement. The number of people on the beach 
contributed significantly to explaining variations in the amount of 
time sanderlings spent feeding, and active feeding time decreased from 
1986 to 1990 (Burger and Gochfeld 1991, p. 263). Along with reduced 
size of prey items, disturbance was a key factor explaining sharp 
declines in red knot food intake rates at R[iacute]o Grande, Argentina, 
on Tierra del Fuego (Escudero et al. 2012, p. 362). Comparing 
conditions in 2008 with earlier studies, total red knot feeding time 
was 0.5 hour shorter due to continuous disturbance and flushing of the 
birds by people, dogs, and ORVs during prime feeding time just after 
high tide (Escudero et al. 2012, pp. 358, 362). Studying another 
Calidris canutus subspecies in Australia, Rogers et al. (2006b, p. 233) 
found that energy expenditure over a tidal cycle was sensitive to the 
amount of disturbance, and a relatively small increase in disturbance 
can result in a substantial increase in energy expenditure. Shorebirds 
may be able to compensate for these costs to some extent by extending 
their food intake, but only to a degree, and such compensation is 
dependent upon the availability of adequate food resources. The 
energetic costs of disturbance are greatest for heavy birds, such as 
just before departure on a migratory flight (Rogers et al. 2006b, p. 
    Both modeling (West et al. 2002, p. 319) and empirical studies 
(Burger 1986, pp. 126-127) suggest that numerous small disturbances are 
generally more costly than fewer, larger disturbances. Burger et al. 
(2007, p. 1164) found that repeated disturbances to red knots and other 
shorebirds may have the effect of increasing interference competition 
for foraging space by giving a competitive advantage to gull species, 
which return to foraging more quickly than shorebirds following a 
response to vehicles, people, or dogs.
    Tarr (2008, p. 133) found that vehicle disturbance decreased the 
amount of

[[Page 60079]]

time that sanderlings spent roosting and resting. Forgues 2010 (pp. 39, 
55) found that shorebirds spent significantly less time foraging and 
more time resting at sites with ORVs, and suggested that the increased 
amount of time spent resting may be a compensation method for energy 
lost from decreased foraging.
    Shorebirds are more likely to be flushed by dogs than by people 
(Thomas et al. 2003, p. 67; Lafferty 2001a, p. 318; Lord et al. 2001, 
p. 233), and birds react to dogs from greater distances than to people 
(Lafferty 2001a, p. 319; Lafferty 2001b, pp. 1950, 1956). Pedestrians 
walking with dogs often go through flocks of foraging and roosting 
shorebirds, and unleashed dogs often chase the birds and can kill them 
(Lafferty 2001b, p. 1955; Burger 1986, p. 128). Burger et al. (2007, p. 
1162) found that foraging shorebirds in migratory habitat do not return 
to the beach following a disturbance by a dog, and Burger et al. 2004 
(pp. 286-287) found that disturbance by dogs is increasing in Delaware 
Bay even as management efforts have been successful at reducing other 
types of disturbances.
    Red knots are exposed to disturbance from recreational and other 
human activities throughout their nonbreeding range. Excessive 
disturbance has been shown to preclude shorebird use of otherwise 
preferred habitats and can impact energy budgets. Both of these effects 
are likely to exacerbate other threats to the red knot, such as habitat 
loss, reduced food availability, asynchronies in the annual cycle, and 
competition with gulls (see Cumulative Effects below).
Factor E--Competition With Gulls
    Gulls foraging on the beaches of Delaware Bay during the red knot's 
spring stopover period may directly or indirectly compete with 
shorebirds for horseshoe crab eggs. Botton (1984, p. 209) noted that, 
in addition to shorebirds, large populations of laughing gulls (Larus 
atricilla) were predominant on New Jersey's horseshoe crab spawning 
beaches along Delaware Bay. Gull breeding colonies in Delaware are not 
located as close to the bayshore beaches as in New Jersey. However, 
immature, large-bodied gulls such as greater black-backed gull and 
herring gull, as well as some laughing gulls, most likely from New 
Jersey breeding colonies, do congregate on the Delaware shore during 
the spring, especially at Mispillion Harbor (Niles et al. 2008, p. 
    Aerial surveys of breeding gull species on the Atlantic coast of 
New Jersey from 1976 to 2007 show that herring and greater black-backed 
gull populations were relatively stable. Greater black-backed gulls 
showed a slight increase in 2001 that had subsided by 2004. Laughing 
gull populations grew steadily from 1976 (fewer than 20,000 birds) to 
1989 (nearly 60,000 birds). Following a dip in 1995, laughing gull 
numbers spiked in 2001 to nearly 80,000. From 2004 to 2007, laughing 
gull numbers returned to approximately the same levels that 
predominated in the 1980s (50,000 to 60,000 birds) (Dey et al. 2011b, 
p. 24).
    From 1992 to 2002, the number of gulls recorded in single-day 
counts on Delaware Bay beaches in New Jersey ranged from 10,000 to 
23,000 (Niles et al. 2008, p. 107). To allow for comparisons, gull 
counts on Delaware Bay were performed in spring 1990 to 1992 and again 
in 2002 using the same methodology (Sutton and Dowdell 2002, p. 3). 
Despite the increasing breeding populations documented by the aerial 
survey of New Jersey's nearby Atlantic coast, gull numbers on Delaware 
Bay beaches were significantly lower in 2002 than they were between 
1990 and 1992. The highest laughing gull count in 2002 was only a third 
of the highest count of the 1990 to 1992 period. When comparing the 
average of the four 1990s counts to the average of the four 2002 
counts, laughing gulls using Delaware Bay beaches declined by 61 
percent decline (Sutton and Dowdell 2002, p. 5). Decreased gull usage 
of Delaware Bay, despite growing regional gull populations, may suggest 
that gulls were responding to reduced availably of horseshoe crab eggs 
by 2002 (Sutton and Dowdell 2002, p. 6).
    Burger et al. (1979, p. 462) found that intraspecific (between 
members of the same species) aggressive interactions of shorebirds were 
more common than interspecific (between members of different species) 
interactions. Negative interactions between red knots and laughing 
gulls that resulted in disruption of knot behavior were no more 
prevalent than interactions with other shorebird species. However, 
larger-bodied species (like gulls) tended to successfully defend areas 
against smaller species. Total aggressive interactions increased as the 
density of birds increased in favored habitats, which indicated some 
competition for food resources (Burger et al. 1979, p. 462).
    Sullivan (1986, pp. 376-377) found that aggression in ruddy 
turnstones increased as experimentally manipulated food resources 
(horseshoe crab eggs) changed from an even distribution to a more 
patchy distribution. Horseshoe crab eggs are typically patchy on 
Delaware Bay beaches, as evidenced by the very high variability of egg 
densities within and between sites (ASMFC 2012d, p. 11). The ruddy 
turnstones' decisions to defend food patches were likely driven by the 
energetic cost of locating new patches (Sullivan 1986, pp. 376-377), 
suggesting that aggression may increase as food availability decreases. 
Botton et al. (1994, p. 609) noted that flocks of shorebirds appeared 
to be deterred from landing on beaches when large flocks of gulls were 
present. When dense, mixed flocks of gulls and shorebirds were 
observed, gulls monopolized the waterline, limiting shorebirds to drier 
sand farther up the beach (Botton et al. 1994, p. 609).
    Following up on earlier studies, Burger (undated, p. 9) studied 
foraging behavior in shorebirds and gulls on the New Jersey side of 
Delaware Bay in spring 2002 to determine if interference competition 
existed between shorebirds and gulls. For red knots, the time devoted 
to foraging when gulls were present was significantly less than when a 
nearest neighbor was any shorebird. Red knots spent more time being 
vigilant when their nearest neighbors were gulls rather than other 
shorebirds. Similarly, red knots engaged in more aggression when gulls 
were nearest neighbors, although they usually lost these encounters 
(Burger undated, p. 10; USFWS 2003, p. 42). The increased vigilance of 
red knots when feeding near gulls comes at the detriment of time spent 
feeding (Niles et al. 2008, p. 107), and red knot foraging efficiency 
is adversely affected by the mere presence of gulls. Hernandez (2005, 
p. 80) found that the foraging efficiency of knots feeding on horseshoe 
crab eggs decreased by as much as 40 percent when feeding close to a 
gull. As described under Background--Species Information--Migration and 
Wintering Food, above, red knots are present in Delaware Bay for a 
short time to replenish energy to complete migration to their arctic 
breeding grounds. Excessive competition from gulls that decreases 
energy intake rates would affect the ability of red knots to gain 
sufficient weight for the final leg of migration.
    Despite the observed competitive behaviors between gulls and red 
knots, Karpanty et al. (2011, p. 992) did not observe red knots to be 
excluded from foraging by aggressive interactions with other red knots, 
other shorebirds, or gull species in experimental sections of beach in 
2004 and 2005. These authors did observe knots foraging in plots with 
high egg densities and knots foraging

[[Page 60080]]

throughout the tidal cycle in all microhabitats. Thus, red knots did 
not appear to be substantially affected by interspecific or 
intraspecific interference competition during this study.
    Burger et al. (2007, p. 1162) found that gulls are more tolerant of 
human disturbance than shorebirds are. When disturbed by humans, gull 
numbers returned to pre-disturbance levels within 5 minutes. Even after 
10 minutes, shorebird numbers failed to reach predisturbance levels. 
Repeated disturbances to red knots and other shorebirds may have the 
effect of increasing interference competition for foraging space by 
giving a competitive advantage to gull species, which return to 
foraging more quickly than shorebirds following a flight response to 
vehicles, people, or dogs (Burger et al. 2007, p. 1164). The size and 
aggression of gulls, coupled with their greater tolerance of human 
disturbance, give gulls a competitive advantage over shorebirds in 
prime feeding areas (Niles et al. 2008, p. 107).
    Reduction of available horseshoe crab eggs or consolidation of 
spawning horseshoe crabs onto fewer beaches can increase interference 
competition among egg foragers. Karpanty et al. (2006, p. 1707) found a 
positive relationship between laughing gull numbers and red knot 
presence (i.e., more laughing gulls were present when red knots were 
also present), concluding that this correlation was likely due to the 
use by both bird species of the sandy beach areas with the highest 
densities of horseshoe crab eggs for foraging. Competition for 
horseshoe crab eggs increases with reduced egg availability, and the 
ability of shorebirds to compete with gulls for food decreases as 
shorebird flock size decreases (Breese 2010, p. 3; Niles et al. 2005, 
p. 4).
    Competition between shorebirds and laughing gulls for horseshoe 
crab eggs increased in the 2000s as the decline in the horseshoe crab 
population concentrated spawning in a few favored areas (e.g., 
Mispillion Harbor, Delaware; Reeds Beach, New Jersey). These ``hot 
spots'' of horseshoe crab eggs concentrated foraging shorebirds and 
gulls, increasing competition for limited resources. Hot spots were 
known to shift in some years when severe wind and rough surf favored 
spawning in sheltered areas (e.g., creek mouths) (Kalasz et al. 2010, 
pp. 11-12). A reduced crab population, the contraction of spawning both 
spatially and temporally, and storm events that concentrated spawning 
into protected creek mouths exacerbated competition for available eggs 
in certain years (Dey et al. 2011b, p. 9). Delaware's shorebird 
conservation plan calls for control of gull populations if they exceed 
a natural size and negatively impact migrating birds (Kalasz 2008, p. 
    In summary, competition with gulls can exacerbate food shortages in 
Delaware Bay. Despite the growth of gull populations in southern New 
Jersey, numbers of gulls using Delaware Bay in spring decreased 
considerably from the early 1990s to the early 2000s. Because more 
recent comparable survey data are not available, we cannot surmise if 
there are any recent trends in competition pressures, nor can we 
project a trend into the future. We conclude that gull competition was 
not a driving cause of red knot population declines in the 2000s, but 
was likely one of several factors (along with predation, storms, late 
arrivals of migrants, and human disturbance) that likely exacerbated 
the effects of reduced horseshoe crab egg availability.
    Gull competition has not been reported as a threat to red knots 
outside of Delaware Bay (e.g., Koch pers. comm. March 5, 2013; Iaquinto 
pers. comm. February 22, 2013), but is likely to exacerbate other 
threats throughout the knot's range due to gulls' larger body sizes, 
high aggression, tolerance of human disturbance, and generally stable 
or increasing populations. However, outside of Delaware Bay, there is 
typically less overlap between the diets of red knots (specializing in 
small, buried, intertidal mollusks) and most gulls species (generalist 
feeders). We expect the effects of gulls to be most pronounced where 
red knots become restricted to reduced areas of foraging habitat, which 
can occur as a result of reduced food resources, human disturbance or 
predation that excludes knots from quality habitats, or outright 
habitat loss (see Cumulative Effects below).
Factor E--Harmful Algal Blooms (HABs)
    A harmful algal bloom (HAB) is the proliferation of a toxic or 
nuisance algal species (which can be microscopic or macroscopic, such 
as seaweed) that negatively affects natural resources or humans 
(Florida Fish and Wildlife Conservation Commission (FFWCC) 2011). While 
most species of microscopic marine life are harmless, there are a few 
dozen species that create toxins given the right conditions. During a 
``bloom'' event, even nontoxic species can disrupt ecosystems through 
sheer overabundance (Woods Hole Oceanographic Institute (Woods Hole) 
2012). The primary groups of microscopic species that form HABs are 
flagellates (including dinoflagellates), diatoms, and blue-green algae 
(which are actually cyanobacteria, a group of bacteria, rather than 
true algae). Of the approximately 85 HAB-forming species currently 
documented, almost all of them are plant-like microalgae that require 
light and carbon dioxide to produce their own food using chlorophyll 
(FFWCC 2011). Blooms can appear green, brown, or red-orange, or may be 
colorless, depending upon the species blooming and environmental 
conditions. Although HABs are popularly called ``red tides,'' this name 
can be misleading, as it includes many blooms that discolor the water 
but cause no harm, while also excluding blooms of highly toxic cells 
that cause problems at low (and essentially invisible) concentrations 
(Woods Hole 2012). Here, we use the term ``red tide'' to refer only to 
blooms of the dinoflagellate Karenia brevis.
HABs--Impacts to Shorebirds
    Large die-offs of fish, mammals, and birds can be caused by HABs. 
Wildlife mortality associated with HABs can be caused by direct 
exposure to toxins, indirect exposure to toxins (i.e., as the toxins 
accumulate in the food web), or through ecosystem impacts (e.g., 
reductions in light penetration or oxygen levels in the water, 
alteration of food webs due to fish kills or other mass mortalities) 
(Woods Hole 2012; Anderson 2007, p. 5; FAO 2004, p. 1). Wildlife can be 
exposed to algal toxins through aerosol (airborne) transport or via 
consumption of toxic prey (FFWCC 2011; Steidinger et al. 1999, p. 6). 
Exposure of wildlife to algal toxins may continue for weeks after an 
HAB subsides, as toxins move through the food web (Abbott et al. 2009, 
p. 4).
    Animals exposed to algal toxins through their diets may die or 
display impaired feeding and immune function, avoidance behavior, 
physiological dysfunction, reduced growth and reproduction, or 
pathological effects (Woods Hole 2012). A poorly defined but 
potentially significant concern relates to sublethal, chronic impacts 
from toxic HABs that can affect the structure and function of 
ecosystems (Anderson 2007, p. 4). Chronic toxin exposure may have long-
term consequences affecting the sustainability or recovery of natural 
populations at higher trophic levels (e.g., species that feed higher in 
the food web). Ecosystem-level effects from toxic algae may be more 
pervasive than yet documented by science, affecting multiple trophic 
levels, depending on the ecosystem and the toxin involved (Anderson 
2007, pp. 4-5).

[[Page 60081]]

    For both humans and shorebirds, shellfish are a key route of 
exposure to algal toxins. When toxic algae are filtered from the water 
as food by shellfish, their toxins accumulate in those shellfish to 
levels that can be lethal to humans or other animals that eat the 
shellfish (Anderson 2007, p. 4). Several shellfish poisoning syndromes 
have been identified according to their symptoms. Those shellfish 
poisoning syndromes that occur prominently within the range of the red 
knot include Amnesic Shellfish Poisoning (ASP) (occurring in Atlantic 
Canada, caused by Pseudo-nitzchia spp.); Neurotoxic Shellfish Poisoning 
(NSP, also called ``red tide'') (occurring on the U.S. coast from Texas 
to North Carolina, caused by Karenia brevis and other species); and 
Paralytic Shellfish Poisoning (PSP) (occurring in Atlantic Canada, the 
U.S. coast in New England, Argentina, and Tierra del Fuego, caused by 
Alexandrium spp. and others) (Woods Hole 2012; FAO 2004, p. 44). The 
highest levels of PSP toxins have been recorded in shellfish from 
Tierra del Fuego (International Atomic Energy Agency 2004), and high 
levels can persist in mollusks for months following a PSP bloom (FAO 
2004, p. 44). In Florida, the St. Johns, St. Lucie, and Caloosahatchee 
Rivers and estuaries have also been affected by persistent HABs of 
cyanobacteria (FFWCC 2011).
    Algal toxins may be a direct cause of death in seabirds and 
shorebirds via an acute or lethal exposure, or birds can be exposed to 
chronic, sublethal levels of a toxin over the course of an extended 
bloom. Sub-acute doses may contribute to mortality due to an impaired 
ability to forage productively, disrupted migration behavior, reduced 
nesting success, or increased vulnerability to predation, dehydration, 
disease, or injury (VanDeventer 2007, p. 1). It is commonly believed 
that the primary risk to shorebirds during an HAB is via contamination 
of shellfish and other invertebrates that constitute their normal diet. 
Coquina clams (Donax variabilis) and other items that shorebirds feed 
upon can accumulate marine toxins during HABs and may pose a risk to 
foraging shorebirds. In addition to consuming toxins via their normal 
prey items, shorebirds have been observed consuming dead fish killed by 
HABs (VanDeventer 2007, p. 11). VanDeventer et al. (2011, p. 31) 
observed shorebirds, including sanderlings and ruddy turnstones, 
scavenging fish killed during a 2005 red tide along the central west 
coast of Florida. Brevetoxins (discussed below) were found both in the 
dead fish and in the livers of dead shorebirds that were collected from 
beaches and rehabilitation centers (VanDeventer et al. 2011, p. 31). 
Although scavenging has not been documented in red knots, clams and 
other red knot prey species are among the organisms that accumulate 
algal toxins.
    Sick or dying birds often seek shelter in dense vegetation; thus, 
those that succumb to HAB exposure are not often observed or 
documented. Birds that are debilitated or die in exposed areas are 
subject to predation or may be swept away in tidal areas. When 
extensive fish kills occur from HABs, the carcasses of smaller birds 
such as shorebirds may go undetected. Some areas affected by HABs are 
remote and rarely visited. Thus, mortality of shorebirds associated 
with HABs is likely underreported.
HABs--Gulf of Mexico
    Algal blooms causing massive fish kills in the Gulf of Mexico have 
been reported anecdotally since the 1500s, but written records exist 
only since 1844. The dinoflagellate Karenia brevis has been implicated 
in producing harmful red tides that occur annually in the Gulf of 
Mexico. Red tides cause extensive marine animal mortalities and human 
illness through the production of highly potent neurotoxins known as 
brevetoxins (FFWCC 2011). Brevetoxins are toxic to fish, marine 
mammals, birds, and humans, but not to shellfish (FAO 2004, p. 137). 
Karenia brevis has come to be known as the Florida red tide organism 
and has also been implicated in HABs in the Carolinas, Alabama, 
Mississippi, Louisiana, and Texas in the United States, as well as in 
Mexico (Marine Genomics Project 2010; Steidinger et al. 1999, pp. 3-4). 
Although red tides can occur throughout the year, most typically start 
from late August through November and last for 4 to 5 months. Red tides 
lasting as long as 21 months have occurred in Florida (FFWCC 2011).
    A red tide event occurred in October 2009 along the Gulf coast of 
Texas during the period that red knots were using the area (Niles et 
al. 2009, Appendix 2). Aerosols produced by the red tide were present 
and affecting human breathing on Padre Island. Over a 2-week period, 
hundreds of thousands of dead fish littered beaches from Mustang 
Island, Texas, south into northern Tamaulipas, Mexico. Most shorebirds 
became conspicuously absent from Gulf coast beaches during that time 
(Niles et al. 2009, p. 5). A red knot that had been captured and banded 
on October 6, 2009, was found 4 days later in poor condition on Mustang 
Island. The bird was captured by hand and taken to an animal 
rehabilitation facility. This bird had been resighted on October 7, the 
day after its original capture, when it was walking normally and 
feeding. At the time of first capture the bird weighed 3.9 oz (113 g); 
its weight on arrival at the rehabilitation facility just 4 days later 
was 2.7 oz (78 g) (Niles et al. 2009, p. 5). While there is no direct 
evidence, the red tide event is suspected as the reason for generally 
low weights and for a sharp decline in weights of red knots captured on 
Mustang Island during October 2009. Not only was the average mass of 
all the knots caught on Mustang Island low compared with other regions, 
but also average weights of individual catches declined significantly 
over the short period of field work (Niles et al. 2009, p. 4), 
coinciding with the red tide event.
    Another Texas red tide event was documented by shorebird biologists 
in October 2011. Over a few days, the observed red knot population 
using Padre Island fell from 150 birds to only a few individuals. 
Captured birds were in extremely poor condition with weights as low as 
2.9 oz (84 g) (Niles 2011c). Researchers picked up six red knots from 
the beach that were too weak to fly or stand and took them to a 
rehabilitator. Two knots that died before reaching the rehabilitation 
facility were tested for brevetoxin concentrations. Liver samples in 
both cases exceeded 2,400 nanograms of brevetoxin per gram of tissue 
(ng/g) (wet weight) (Newstead et al. in press). These levels are 
extremely high (Newstead et al. in press; Atwood 2008, p. 27). Samples 
from muscle and gastrointestinal tracts were also positive for 
brevetoxin, but at least an order of magnitude lower than in the 
livers. An HAB expert concluded that brevetoxins accounted for the 
mortality of these red knots (Newstead et al. in press). Whether the 
toxin was taken up by the birds through breathing or via consumption of 
contaminated food is unclear. However, other shorebird species that do 
not specialize on mollusks (especially sanderling and ruddy turnstone) 
were present during the red tide but did not appear to be affected by 
brevetoxins. This observation suggests uptake in the red knots may have 
been related to consumption of clams that had accumulated the toxin. In 
the case of this red tide event, the outbreak was confined to the Gulf 
beaches, but Karenia brevis is capable of spreading into bay habitats 
(e.g., Laguna Madre) as well. Red knots are apparently vulnerable to 
red tide toxins, so a widespread outbreak could significantly

[[Page 60082]]

diminish the amount of available habitat (Newstead et al. in press).
    Although no HAB-related red knot mortality has been reported from 
Florida, HABs have become a common feature of Florida's coastal 
environment and are associated with fish, invertebrate, bird, manatee, 
and other wildlife kills (Abbott et al. 2009, p. 3; Steidinger et al. 
1999, pp. v, 3-4). Red tides occur nearly every year along Florida's 
Gulf coast, and may affect hundreds of square miles (FFWCC 2011). Red 
tides are most common off the central and southwestern coasts of 
Florida between Clearwater and Sanibel Island (FFWCC 2011), which 
constitute a key portion of the red knot's Southeast wintering area 
(Niles 2009, p. 4; Niles et al. 2008, p. 17). Brevitoxins from red 
tides accumulate in mollusks such as the small coquina clams that red 
knots are known to forage on in Florida. Reports of dead birds during 
red tide events are not unusual but are not well documented in the 
scientific literature. More often, red tides are documented by reports 
of fish kills, which can be extensive (FFWCC 2011).
    In April 2007, 312 red knots were found dead on the coast of 
southeastern Uruguay at Playa La Coronilla. Another 1,000 dead 
shorebirds were found nearby on the same day, also in southeastern 
Uruguay, but could not be confirmed to be red knots. Local bird experts 
suspected that the shorebird mortality event could be related to an HAB 
(BirdLife International 2007). However, the cause of death could not be 
determined, and no connection with an HAB could be established (J. 
Aldabe pers. comm. February 4, 2013). Red knots passing through Uruguay 
in April would be expected to be those that had wintered in Tierra del 
Fuego. A die-off of up to 1,300 red knots would account in large part 
for the 15 percent red knot decline observed in Tierra del Fuego in 
winter 2008.
HABs--Causes and Trends
    During recent decades, the frequency, intensity, geographic 
distribution, and impacts of HABs have increased, along with the number 
of toxic compounds found in the marine food chain (Anderson 2007, p. 2; 
FAO 2004, p. 2). Coastal regions throughout the world are now subject 
to an unprecedented variety and frequency of HAB events. Many countries 
are faced with a large array of toxic or harmful species, as well as 
trends of increasing bloom incidence, larger areas affected, and more 
marine resources impacted. The causes behind this expansion are 
debated, with possible explanations ranging from natural mechanisms of 
species dispersal and enhancement to a host of human-related phenomena 
including climate change (Anderson 2007, pp. 3, 13; FAO 2004, p. 2). 
The influence of human activities in coastal waters may allow HABs to 
extend their ranges and times of residency (Steidinger et al. 1999, p. 
    Some new bloom events reflect indigenous algal populations 
discovered because of better detection methods and more observers. 
Several other ``spreading events'' are most easily attributed to 
natural dispersal via currents, rather than human activities (Anderson 
2007, p. 11). However, human activities have contributed to the global 
HAB expansion by transporting toxic species in ship ballast water 
(Anderson 2007, p. 13). Another factor contributing to the global 
expansion in HABs is the substantial increase in aquaculture activities 
in many countries (Anderson 2007, p. 13), and the transfer of shellfish 
stocks from one area to another (FAO 2004, p. 2). Changed land use 
patterns, such as deforestation, can also cause shifts in phytoplankton 
species composition by increasing the concentrations of organic matter 
in land runoff. Acid precipitation can further increase the mobility of 
organic matter and trace metals in soils (FAO 2004, p. 1), which 
contribute to creating environmental conditions suitable for HABs.
    Of the causal factors leading to HABs, excess nutrients often 
dominate the discussion (Steidinger et al. 1999, p. 2). Coastal waters 
are receiving large and increasing quantities of industrial, 
agricultural, and sewage effluents through a variety of pathways. In 
many urbanized coastal regions, these anthropogenic inputs have altered 
the size and composition of the nutrient pool which may, in turn, 
create a more favorable nutrient environment for certain HAB species 
(Anderson 2007, p. 13). Shallow and restricted coastal waters that are 
poorly flushed appear to be most susceptible to nutrient-related algal 
problems. Nutrient enrichment of such systems often leads to excessive 
production of organic matter (a process known as eutrophication) and 
increased frequencies and magnitudes of algal blooms (Anderson 2007, p. 
    On a global basis, Anderson et al. (2002, p. 704) found strong 
correlations between total nitrogen input and phytoplankton production 
in estuarine and marine waters. There are also numerous examples of 
geographic regions (e.g., Chesapeake Bay, North Carolina's Albemarle-
Pamlico Sound) where increases in nutrient loading have been linked 
with the development of large biomass blooms, leading to oxygen 
depletion and even toxic or harmful impacts on marine resources and 
ecosystems. Some regions have witnessed reductions in phytoplankton 
biomass or HAB incidence upon implementation of nutrient controls. 
Shifts in algal species composition have often been attributed to 
changes in the ratios of various nutrients (nitrogen, phosphorous, 
silicon) (Anderson et al. 2002, p. 704), and it is possible that algal 
species that are normally not toxic may be rendered toxic when exposed 
to atypical nutrient regimes resulting from human-caused eutrophication 
(FAO 2004, p. 1). The relationships between nutrient delivery and the 
development of blooms and their potential toxicity or harmfulness 
remain poorly understood. Due to the influence of several environmental 
and ecological factors, similar nutrient loads do not have the same 
impact in different environments, or in the same environment at 
different times. Eutrophication is one of several mechanisms by which 
harmful algae appear to be increasing in extent and duration in many 
locations (Anderson et al. 2002, p. 704).
    Although important, eutrophication is not the only explanation for 
algal blooms or toxic outbreaks (Anderson et al. 2002, p. 704). The 
link is clear between nutrients and nontoxic algal blooms, which can 
cause oxygen depletion in the water, fish kills, and other ecosystem 
impacts (Woods Hole 2012; Anderson 2007, p. 5; Anderson et al. 2002, p. 
704; Steidinger et al. 1999, p. 2). However, the connection with excess 
nutrients is less clear for algal species that produce toxins, as toxic 
blooms can begin in open water miles away from shore or the immediate 
influence of human activities (Steidinger et al. 1999, p. 2). Many of 
the new or expanded HAB problems have occurred in waters with no 
influence from pollution or other anthropogenic effects (Anderson 2007, 
pp. 11, 13).
    The overall effect of nutrient overenrichment on harmful algae is 
species specific. Nutrient enrichment has been strongly linked to 
stimulation of some harmful algal species, but for others it has 
apparently not been a contributing factor (Anderson et al. 2002, p. 
704). There is no evidence of a direct link between Florida red tides 
and nutrient pollution (FFWCC 2011). Elevated nutrients in inshore 
areas do not start these blooms but, in some instances, can allow a 
bloom to persist in the nutrient-rich environment for a slightly longer 
period than normal (Steidinger et al. 1999, p. 2). For those

[[Page 60083]]

regions and algal species where nutrient enrichment is a causative or 
contributing factor, increased coastal water temperatures and greater 
spring runoff associated with global warming may increase the frequency 
of HABs (USGCRP 2009, pp. 46, 150).
    Coastal managers are working toward mitigation, prevention, and 
control of HABs. Mitigation efforts are typically focused on protecting 
human health (Anderson 2007, p. 15), and are thus unlikely to prevent 
exposure of red knots. Several challenges hinder prevention efforts, 
including lack of information regarding the factors that cause blooms 
and limitations on the extent to which those factors can be modified or 
controlled (Anderson 2007, p. 16). Bloom control is the most 
challenging and controversial aspect of HAB management. Control refers 
to actions taken to suppress or destroy HABs, directly intervening in 
the bloom process. There are five categories or strategies that can be 
used to combat or suppress an invasive or harmful species, consisting 
of mechanical, biological, chemical, genetic, and environmental 
control. Several of these methods have been applied to HAB species 
(Anderson 2007, p. 18). However, the science behind HAB control is 
rudimentary and slow moving, and most control methods are currently 
infeasible, theoretical, or only possible on an experimental scale 
(Anderson 2007, pp. 18-20). It is likely that HABs will always be 
present in the coastal environment and, in the next few decades at 
least, are likely to continue to expand in geographic extent and 
frequency (Anderson 2007, p. 2).
    To date, direct impacts to red knots from HABs have been documented 
only in Texas, although a large die-off in Uruguay may have also been 
linked to an HAB. We conclude that some level of undocumented red knot 
mortality from HABs likely occurs most years, based on probable 
underreporting of shorebird mortalities from HABs and the direct 
exposure of red knots to algal toxins (particularly via contaminated 
prey) throughout the knot's nonbreeding range. We have no documented 
evidence that HABs were a driving factor in red knot population 
declines in the 2000s. However, HAB frequency and duration have 
increased and do not show signs of abating over the next few decades. 
Combined with other threats, ongoing and possibly increasing mortality 
from HABs may affect the red knot at the population level.
Factor E--Oil Spills and Leaks
    The red knot has the potential to be exposed to oil spills and 
leaks throughout its migration and wintering range. Oil, as well as 
spill response activities, can directly and indirectly affect both the 
bird and its habitat through several pathways. Red knots can be exposed 
to petroleum products via spills from shipping vessels, leaks or spills 
from offshore oil rigs or undersea pipelines, leaks or spills from 
onshore facilities such as petroleum refineries and petrochemical 
plants, and beach-stranded barrels and containers that can fall from 
moving cargo ships or offshore rigs. Several key red knot wintering or 
stopover areas also contain large-scale petroleum extraction, 
transportation, or both activities. With regard to potential effects on 
red knot habitats, the geographic location of a spill, weather 
conditions (e.g., prevailing winds), and type of oil spilled are as 
important, if not more so, than the volume of the discharge.
    Petroleum oils are complex and variable mixtures of many chemicals 
and include crude oils and their distilled products that are 
transported globally in large quantities. Overwhelming evidence exists 
that petroleum oils are toxic to birds (Leighton, 1991, p. 43). Acute 
exposure to oil can result in death from hypothermia (i.e., from loss 
of the feathers' waterproofing and insulating capabilities), 
smothering, drowning, dehydration, starvation, or ingestion of toxins 
during preening (Henkel et al. 2012, p. 680; Peterson et al. 2003, p. 
2085). In shorebirds, oil ingestion by foraging in contaminated 
intertidal habitats and consumption of contaminated prey may also be a 
major contamination pathway (Henkel et al. 2012, p. 680; Peterson et 
al. 2003, p. 2083). Mortality from ingested oil is primarily associated 
with acute toxicity involving the kidney, liver, or gastrointestinal 
tract (Henkel et al. 2012, p. 680; Leighton 1991, p. 46). In addition 
to causing acute toxicity, ingested oil can induce a variety of 
toxicologically significant systemic effects (Leighton 1991, p. 46). 
Since shorebird migration is energetically and physiologically 
demanding, the sublethal effects of oil may have severe consequences 
that lead to population-level effects (Henkel et al. 2012, p. 679). Oil 
can have long-term effects on populations through compromised health of 
exposed animals and chronic toxic exposures from foraging on 
persistently contaminated prey or habitats (Peterson et al. 2003, p. 
    Oiled birds may also experience decreased foraging success due to a 
decline in prey populations following a spill or due to increased time 
spent preening to remove oil from their feathers (Henkel et al. 2012, 
p. 681). Shorebirds oiled during the 1996 T/V Anitra spill in Delaware 
Bay showed significant negative correlations between the amount of 
oiling and foraging behaviors, and significant positive correlations 
between oiling and time spent standing and preening (Burger 1997a, p. 
293). Moreover, oil can reduce invertebrate abundance or alter the 
intertidal invertebrate community that provides food for shorebirds 
(Henkel et al. 2012, p. 681; USFWS 2012a, p. 35). The resulting 
inadequate weight gain and diminished health may delay birds' 
departures, decrease their survival rates during migration, or reduce 
their reproductive fitness (Henkel et al. 2012, p. 681). In addition, 
reduced abundance of a preferred food may cause shorebirds to move and 
forage in other, potentially lower quality, habitats (Henkel et al. 
2012, p. 681; USFWS 2012a, p. 35). Prey switching has not been 
documented in shorebirds following an oil spill (Henkel et al. 2012, p. 
681). However shorebirds including red knots are known to switch 
habitats in response to disturbance (Burger et al. 1995, p. 62) and to 
switch prey types if supplies of the preferred prey are insufficient 
(Escudero et al. 2012, pp. 359, 362). A bird's inability to obtain 
adequate resources delays its premigratory fattening and can delay the 
departure to the breeding grounds; birds arriving on their breeding 
grounds later typically realize lower reproductive success (see 
Asynchronies, above) (Henkel et al. 2012, p. 681; Gunnarsson et al. 
2005, p. 2320; Myers et al. 1987, pp. 21-22).
    Finally, efforts to prevent shoreline oiling and cleanup response 
activities can disturb shorebirds and their habitats (USFWS 2012a, p. 
36; Burger 1997a, p. 293; Philadelphia Area Committee 1998, Annex E). 
Movement of response personnel on the beach and vessels in the water 
can flush both healthy and sick birds, causing disruptions in feeding 
and roosting behaviors (see Human Disturbance, above). In addition to 
causing disturbance, post-spill beach cleaning activities can impact 
habitat suitability and prey availability (see Factor A--Beach 
Cleaning, above). And lastly, dispersants used to break up oil can also 
have health effects on birds (NRC 2005, pp. 254-257).
Oil Spills--Canada
    The shorebird habitats of the Mingan Islands in the Gulf of St. 

[[Page 60084]]

(Province of Quebec) are at risk from oil impacts because of their 
proximity to ships carrying oil through the archipelago to the Havre-
Saint-Pierre harbor (Niles et al. 2008, p. 100). In March 1999, one 
ship spilled 40 tons (44 metric tons) of bunker fuel that washed ashore 
in the Mingan area. Oil from the 1999 spill did reach the islands used 
as a red knot foraging and staging area, but no information is 
available about the extent of impacts to prey species from the oil 
spill (USFWS 2011b, p. 23). If a similar accident were to occur during 
the July to October stopover period, it could have a serious impact on 
the red knots and their feeding areas (USFWS 2011b, p. 23; Niles et al. 
2008, p. 100). In addition, some of the roughly 7,000 vessels per year 
that transit the St. Lawrence seaway illegally dump bilge waste water, 
which is another source of background-level oil and contaminant 
pollution affecting red knot foraging habitat and prey resources within 
the Mingan Island Archipelago (USFWS 2011b, p. 23). However, we have no 
specific information on the extent or severity of this contamination.
Oil Spills--Delaware Bay
    The Delaware Bay and River are among the largest shipping ports in 
the world, especially for oil products (Clark in Farrell and Martin 
1997, p. 24), and home to the fifth largest port complex in the United 
States in terms of total waterborne commerce (Philadelphia Area 
Committee 1998, Annex E). Every year, over 70 million tons of cargo 
move through the tri-state port complex, which consists of the ports of 
Philadelphia, Pennsylvania; Camden, Gloucester City, and Salem, New 
Jersey; and Wilmington, Delaware. This complex is the second largest 
U.S. oil port, handling about 85 percent of the east coast's oil 
imports (Philadelphia Area Committee 1998, Annex E).
    The farthest upstream areas of Delaware Bay used by red knots 
(Niles et al. 2008, p. 43) are about 30 river miles (48 river km) 
downstream of the nearest port facilities, at Wilmington, Delaware. 
However, all vessel traffic must pass through the bay en route to and 
from the ports. In general, high-risk areas are where the greatest 
concentrations of chemical facilities are located, as major pollution 
incidents have typically occurred in locations where quantities of 
pollutant materials are stored, processed, or transported. Several 
areas considered high risk by the USCG are within the region used by 
red knots during spring migration, including Port Mahon and the Big 
Stone Beach Anchorage in Delaware, and the Delaware Bay and its 
approaches (Philadelphia Area Committee 1998, Annex E).
    The narrow channel and frequent occurrence of strong wind and tide 
conditions increase the risk of oil spills in the Delaware River or Bay 
(Clark in Farrell and Martin 1997, p. 24); however, maritime accidents 
and groundings also frequently occur in fair weather and calm seas. 
Because the river is tidal, plumes of discharged material can spread 
upstream and downstream depending upon the tide. Generally, pollutants 
in the river travel proximally 4 mi (6.4 km) upstream during the flood 
cycle, and 5 mi (8 km) downstream during the ebb cycle. Wind direction 
and speed also play important roles in oil movement while free-floating 
oil remains on the water. As the Delaware River and upper bay are long 
and narrow, any medium or large spills are likely to affect both banks 
for several miles up and down the shorelines. In addition to direct 
spill effects, indirect impacts may occur during control of vessel 
traffic during a discharge, which can cause visual and noise 
disturbance to local wildlife, particularly shoreline-foraging species 
(Philadelphia Area Committee 1998, Annex E).
    Although there have been several thousand spills reported in the 
Delaware River since 1986, the average release was only about 150 
gallons (gal) (568 liters (L)) per spill. Less than 1 percent of all 
spills in the port are greater than 10,000 gal (37,854 L). Table 10 
shows the history of spills greater than 10,000 gal (37,854 L) in the 
port since 1985. Based on the history of spills in the Delaware River, 
a release of 200,000 to 500,000 gal (757,082 to 1.9 million L) of oil 
is the maximum that would be expected during a major incident. Major 
oil spills on the Delaware River to date have been less than the 
maximum. There is no known history of significant tank failures 
(discharges) in the port, although tank fires and explosions have been 
documented (Philadelphia Area Committee 1998, Annex E).

    Table 10--Oil Spills Greater Than 10,000 Gallons (37,854 Liters) in the Delaware River and Bay Since 1985
                                                  [NOAA 2013d]
                                                            Volume                                  river miles
                Vessel                       Date          (gallons)            Location          from Red  Knot
M/V Athos 1...........................      11/12/2004         265,000  Paulsboro, NJ...........              45
T/V Anitra............................        5/9/1996          42,000  Big Stone Anchorage, DE.               0
T/V Presidente Rivera.................       6/24/1989         306,000  Marcus Hook, NJ.........              40
T/V Grand Eagle.......................       9/28/1985         435,000  Marcus Hook, NJ.........              40
T/V Mystra............................       9/18/1985          10,000  Delaware Bay............               0

    Although the Anitra spill occurred in May near red knot habitat, 
environmental conditions caused the oil to move around the Cape May 
Peninsula to the Atlantic coast of New Jersey by the second half of 
May. Thus, oil contamination of the bayshores was minimal during the 
period when the greatest concentrations of red knots were present in 
Delaware Bay (Burger 1997a, p. 291). However, unusually large numbers 
of shorebirds fed on the Atlantic coast in the spring of 1996 because 
cold waters delayed the horseshoe crab spawn in Delaware Bay (Burger 
1997a, p. 292), thus increasing the number of birds exposed to the oil. 
These circumstances underscore the importance of spill location and 
environmental conditions, not just merely spill volume, in determining 
the impacts of a spill on red knots. Although red knots were present in 
at least one oiled location (Ocean City, New Jersey) (Burger 1997a, p. 
292) and at least a few knots were oiled (J. Burger pers. comm. March 
5, 2013), the vast majority of impacts were to sanderlings and other 
shorebird species (Anitra Natural Resource Trustees 2004, p. 5).
    Large spills upriver, or moderate spills in the upper bay, have the 
potential to contact a significant portion of the shorebird 
concentration areas. Although the migration period when crabs and 
shorebirds are present is

[[Page 60085]]

short, even a minor spill (i.e., less than 1,000 gal (3,785 L)) could, 
depending on the product spilled, affect beach quality for many years. 
Both New Jersey and Delaware officials work closely with Emergency 
Response managers and the USCG in planning for such an occurrence 
(Kalasz 2008, pp. 39-40; Clark in Farrell and Martin 1997, p. 24).
Oil Spills--Gulf of Mexico
    As of 2010, there were 3,409 offshore petroleum production 
facilities in Federal waters within the Gulf of Mexico Outer 
Continental Shelf (OCS), down from 4,045 in 2001 (Bureau of Safety and 
Environmental Enforcement (BSEE) undated). Gulf of Mexico Federal 
offshore operations account for 23 percent of total U.S. crude oil 
production and 7 percent of total U.S. natural gas production. Over 40 
percent of the total U.S. petroleum refining capacity, as well as 30 
percent of the U.S. natural gas processing plant capacity, is located 
along the Gulf coast. Total liquid fuels production in 2011 was 10.3 
million barrels per day (U.S. Energy Information Administration 2013). 
For the entire Gulf of Mexico region, total oil production in 2012 was 
425 million barrels, down from 570 million barrels in 2009 (BSEE 2013).
    The BSEE tracks spill incidents of one barrel or greater in size of 
petroleum and other toxic substances resulting from Federal OCS oil and 
gas activities (BSEE 2012). Table 11 shows the number of spills 50 
barrels (2,100 gal (7,949 L)) or greater in the Gulf of Mexico since 
1996. These figures do not include incidents stemming from substantial 
extraction operations in State waters. Crude oil production in 2012 was 
an estimated 4.9 million barrels in Louisiana State waters (Louisiana 
Department of Natural Resources 2013), and over 272,000 barrels in 
Texas State waters (Railroad Commission of Texas 2013). In Louisiana, 
about 2,500 to 3,000 oil spills are reported in the Gulf region each 
year, ranging in size from very small to thousands of barrels (USFWS 
2012a, p. 37).

  Table 11--Federal Outer Continental Shelf Spill Incidents 50 Barrels
  (2,100 Gallons (7,949 liters)) or Greater, Resulting From Oil and Gas
                        Activities, 1996 to 2012
                               [BSEE 2012]
                                                              Number of
                            Year                              incidents
2012.......................................................            8
2011.......................................................            3
2010.......................................................            5
2009.......................................................           11
2008.......................................................           33
2007.......................................................            4
2006.......................................................           14
2005.......................................................           49
2004.......................................................           22
2003.......................................................           12
2002.......................................................           12
2001.......................................................            9
2000.......................................................            7
1999.......................................................            5
1999.......................................................            9
1997.......................................................            3
1996.......................................................            3

    Nationwide, spill rates (the number of incidents per billion 
barrels of crude oil handled) in several sectors decreased or remained 
stable over recent decades. From 1964 to 2010, spill rates declined for 
OCS pipelines, and spill rates from tankers decreased substantially, 
probably because single-hulled tankers were largely phased out (see the 
``International Laws and Regulations'' section of the Factor D 
supplemental document). Looking at the whole period from 1964 to 2010, 
nationwide spill rates for OCS platforms were unchanged for spills 
1,000 barrels or greater, and decreased for spills 10,000 barrels or 
greater. However, spill rates at OCS platforms increased in the period 
1996 to 2010 relative to the period 1985 to 1999, as the later period 
included several major hurricanes (e.g., Hurricane Katrina and 
Hurricane Rita) and the Deepwater Horizon spill (Anderson et al. 2012, 
pp. iii-iv). Generally decreasing spill rates were partially offset by 
increasing production, as shown in Table 12.

                    Table 12--Nationwide Outer Continental Shelf Petroleum Production, and Spills 1 Barrel or Greater, 1964 to 2009 *
                                                              [Anderson et al. 2012, p. 10]
                                                                               Barrels spilled by spill size          Number of spills by spill size
                                       Barrels spilled
                Year                     per billion       Billions of       Total     1 to 999    1,000 Barrels     Total     1 to 999    1,000 Barrels
                                      barrels produced  barrels produced                Barrels     or greater                  barrels     or Greater
1964-1970...........................           255,280              1.54     394,285       3,499         390,786          33          23              10
1971-1990...........................            16,682              6.79     113,307      21,415          91,892       1,921       1,909              12
1991-2009...........................             6,427               9.2      59,142      28,144          30,998         853         843              10
1964-2009...........................            32,329             17.53     566,734      53,058         513,676       2,807       2,775              32
* Spill data for 1964 to 1970 are for spills of 50 barrels or greater. Barrels of production or spillage may not add due to rounding of decimals not
  shown. One barrel equals 42 gallons (159 liters).

    In the Gulf of Mexico, threats from oil spills are primarily from 
the high volume of shipping vessels, from which most documented spills 
have originated, traveling offshore and within connected bays. In 
addition to the risk of leaks and spills from offshore oil rigs, 
pipelines, and petroleum refineries, there is a risk of leaks from oil-
filled barrels and containers that routinely wash up on the Texas 
coast. Federal and State land managers have protective provisions in 
place to secure and remove the barrels, thus reducing the likelihood of 
contamination (M. Bimbi pers. comm. November 1, 2012).
    Chronic spills of oil from rigs and pipelines and natural seeps in 
the Gulf of Mexico generally involve small quantities of oil. The oil 
from these smaller leaks and seeps, if they occur far enough from land, 
tend to wash ashore as tar balls. In cases such as this, the impact is 
limited to discrete areas of the beach, whereas oil slicks from larger 
spills coat longer stretches of the shoreline. In late July and early 
August 2009, for example, oil suspected to have originated from an 
offshore oil rig in Mexican waters was observed on 14

[[Page 60086]]

piping plovers in south Texas (USFWS 2012a, p. 37). Mexican waters were 
not included in the oil and gas production or spill statistics given 
    On April 20, 2010, an explosion and fire occurred on the mobile 
offshore drilling unit Deepwater Horizon, which was being used to drill 
a well in the Macondo prospect (Mississippi Canyon 252) (Natural 
Resource Trustees 2012, p. 7). The rig sank and left the well releasing 
tens of thousands of barrels of oil per day into the Gulf of Mexico. It 
is estimated that 5 million barrels (210 million gal (795 million L)) 
of oil were released from the Macondo wellhead. Of that, approximately 
4.1 million barrels (172 million gal (651 million L)) of oil were 
released directly into the Gulf of Mexico over nearly 3 months. In what 
was the largest and most prolonged offshore oil spill in U.S. history, 
oil and dispersants impacted all aspects of the coastal and oceanic 
ecosystems (Natural Resource Trustees 2012, p. 7). At the end of July 
2010, approximately 625 mi (1,006 km) of Gulf of Mexico shoreline were 
oiled. By the end of October, 93 mi (150 km) were still affected by 
moderate to heavy oil, and 483 mi (777 km) of shoreline were affected 
by light to trace amounts of oil (USFWS 2012a, p. 36; Unified Area 
Command 2010). These numbers reflect weekly snapshots of shorelines 
experiencing impacts from oil and do not include cumulative impacts or 
shorelines that had already been cleaned (M. Bimbi pers. comm. November 
1, 2012; USFWS 2012a, p. 36). Limited cleanup operations were still 
ongoing throughout the spill area in November 2012 (USFWS 2012a, p. 
36). A Natural Resources Damage Assessment (NRDA) to assess injury to 
wildlife resources is in progress (Natural Resource Trustees 2012, pp. 
8-9), but due to the legal requirements of the NRDA process, avian 
injury information, including any impacts to red knots, has not been 
released (P. Tuttle pers. comm. November 8, 2012).
Oil Spills--South America
South America--Brazil and Patgonia
    Threats to red knot habitat in Maranh[atilde]o, Brazil include oil 
pollution as well as habitat loss (see Factor A above) from offshore 
petroleum exploration on the continental shelf (WHSRN 2012; Niles et 
al. 2008, p. 97; COSEWIC 2007, p. 37).
    Oil pollution is also a threat at several red knot wintering and 
stopover habitats along the Patagonian coast of Argentina including 
Pen[iacute]nsula Vald[eacute]s and Bah[iacute]a Bustamante; at the 
latter site, 15 percent of red knots were polluted with oil during a 
study in 1979 (Niles et al. 2008, p. 98). Further south in Argentina, 
at a shorebird reserve and red knot stopover area in R[iacute]o 
Gallegos near Tierra del Fuego, the main threat comes from oil and coal 
transport activities. Crude oil and coal are loaded onto ships at a 
hydrocarbon port where the estuary empties into the sea adjacent to the 
salt marsh zone. This area has a history of oil tankers running aground 
because of extreme tides, strong winds, tidal currents, and piloting 
errors. A shipwreck at R[iacute]o Gallegos could easily contaminate key 
areas used by shorebirds, including red knots (WHSRN 2012; Niles et al. 
2008, p. 98; Ferrari et al. 2002, p. 39). However, oil pollution has 
decreased significantly along the Patagonian coast (Niles et al. 2008, 
p. 98).
South America--Tierra del Fuego
    The risk of an oil spill is a primary threat to the largest red 
knot wintering areas in both the Chilean and Argentinean portions of 
Tierra del Fuego (WHSRN 2012; Niles et al. 2008, pp. 98-99; COSEWIC 
2007, p. 36) due to the proximity of large-scale oil operations close 
to key red knot habitats. In recent years, oil operations have been 
decreasing in Chile around Bah[iacute]a Lomas, but increasing along the 
Argentinean coast of Tierra del Fuego (Niles et al. 2008, p. 98; 
COSEWIC 2007, pp. 36-37).
    The region of Magellan, Chile, has traditionally been an important 
producer of oil and natural gas since the first oil discovery was made 
in 1945 within 6.2 mi (10 km) of the bayshore, in Manantiales. 
Production continues, although local oil activity has diminished over 
the last 20 years. Oil is extracted by drilling on land and offshore, 
the latter with no new drillings between 2000 and 2008. The largest 
single red knot wintering site, Bah[iacute]a Lomas, has several oil 
platforms. Most are static, and several were closed around 2007 as the 
oil resource had been depleted (Niles et al. 2008, p. 98). However, the 
red knot area at Bah[iacute]a Lomas remains at risk from a spill or 
leak from the remaining oil extraction facilities.
    Exposure of red knots to hydrocarbon pollution at Bah[iacute]a 
Lomas could also come from shipping accidents, as the site is located 
at the eastern end of the Strait of Magellan, an area historically 
characterized by high maritime shipping traffic (WHSRN 2012). Two oil 
spills from shipping have been recorded near the Strait of Magellan 
First Narrows (immediately west of Bah[iacute]a Lomas), one involving 
53,461 tons (48,500 metric tons) in 1974 and one involving 99 tons (90 
metric tons) in 2004 (Niles et al. 2008, p. 98; COSEWIC 2007, p. 36). 
No incidents have been reported of red knots being affected by 
substantial oiling of the plumage or effects to the prey base. However, 
small amounts of oil have been noted on some red knots caught during 
banding operations (Niles et al. 2008, p. 98; COSEWIC 2007, p. 36).
    In 10 of the 12 years since 2000 for which survey data are 
available, Bah[iacute]a Lomas supported over half of the total 
Argentina-Chile wintering population of red knots, rising to over 90 
percent from 2010 through 2012 (G. Morrison pers. comm. August 31, 
2012). Thus, a significant spill (or several small spills) has the 
potential to substantially impact red knot populations, depending on 
the timing and severity of oil contamination within red knot habitats. 
The National Oil Company extracts, transports, and stores oil in the 
area next to Bah[iacute]a Lomas and has been an important and 
cooperative partner in conservation of the bay (WHSRN 2012), including 
recent efforts to develop a management plan for the area (Niles in 
Ydenberg and Lank 2011, p. 198).
    On the nearby Atlantic Ocean coast of Argentinean Tierra del Fuego, 
oil drilling increased around 1998 (Niles et al. 2008, p. 98; COSEWIC 
2007, pp. 36-37). In the Argentina portion of Tierra del Fuego, 
Bah[iacute]a San Sebasti[aacute]n is the area most vulnerable from oil 
and gas operations that occur on lands near the coast and beach. 
Bah[iacute]a San Sebasti[aacute]n is surrounded by hundreds of oil 
wells (Gappa and Sueiro 2007, p. 680). An 18-in (46-cm) pipe submerged 
in the bay runs 2.9 mi (4.5 km) out to a buoy anchored to the seabed 
(WHSRN 2012). The pipe is used to load crude oil onto tankers bound for 
various distilleries in the country (WHSRN 2012; Gappa and Sueiro 2007, 
p. 680). Wind velocities over 37 mi per hour (60 km per hour) typically 
occur for 200 days of the year, and loading and transport of 
hydrocarbons often take place during rough seas. Thus, an oil spill is 
a persistent risk and could have long-term effects (Gappa and Sueiro 
2007, p. 680). While companies have strict security controls, this 
activity remains a potential threat to shorebirds in the area (WHSRN 
    Farther south on Tierra del Fuego, the area near the shorebird 
reserves at R[iacute]o Grande, Argentina, is important for onshore and 
offshore oil production, which could potentially contribute to oil 
pollution, especially from oil tankers loading around R[iacute]o Grande 
City. No direct evidence exists of red knots being affected by oil 
pollution, but it remains a risk (Niles et al. 2008, pp. 98-99).

[[Page 60087]]

Oil Spills--Summary
    Red knots are exposed to large-scale petroleum extraction and 
transportation operations in many key wintering and stopover habitats 
including Tierra del Fuego, Patagonia, the Gulf of Mexico, Delaware 
Bay, and the Gulf of St. Lawrence. To date, the documented effects to 
red knots from oil spills and leaks have been minimal; however, 
information regarding any oiling of red knots during the Deepwater 
Horizon spill has not yet been released. We conclude that high 
potential exists for small or medium spills to impact moderate numbers 
of red knots or their habitats, such that one or more such events is 
likely over the next few decades, based on the proximity of key red 
knot habitats to high-volume oil operations. Risk of a spill may 
decrease with improved spill contingency planning, infrastructure 
safety upgrades, and improved spill response and recovery methods. 
However, these decreases in risk (e.g., per barrel extracted or 
transported) could be offset if the total volume of petroleum 
extraction and transport continues to grow. A major spill affecting 
habitats in a key red knot concentration area (e.g., Tierra del Fuego, 
Gulf coasts of Florida or Texas, Delaware Bay, Mingan Archipelago) 
while knots are present is less likely but would be expected to cause 
population-level impacts.
Factor E--Environmental Contaminants
    Environmental contaminants can have profound effects on birds, 
acting from the molecular through population levels (Rattner and 
Ackerson 2008, p. 344). Little experimental work has been done on the 
toxic effects of organochlorines (e.g., polychlorinated biphenyls 
(PCBs); pesticides such as DDT (dichloro-diphenyl-trichloroethane), 
dieldrin, and chlordane) or trace elements (e.g., mercury, cadmium, 
arsenic, selenium) in shorebirds, but adult mortality due to 
organochlorine poisoning has been recorded (Braune and Noble 2009, pp. 
    In 1991 and 1992, Braune and Noble (2009, p. 185) tested 12 
shorebird species (not including Calidris canutus) from 4 sites across 
Canada (including 2 red knot stopover areas) for PCBs, organochlorine 
pesticides, mercury, selenium, cadmium, and arsenic. Contaminant 
exposure among species varied with diet, foraging behavior, and 
migration patterns. Diet composition seemed to provide a better 
explanation for contaminant exposure than bill length or probing 
behaviors. Based on the concentrations measured, researchers found no 
indication that contaminants were adversely affecting the shorebird 
species sampled in this study (Braune and Noble 2009, p. 201).
    Heavy shipping traffic in the Gulf of St. Lawrence (Province of 
Quebec) presents a risk of environmental contamination, as well as 
possible oil spills (which were discussed above). Red knot habitats in 
the Mingan Islands are particularly at risk because large ships 
carrying titanium and iron navigate through the archipelago to the 
Havre-Saint-Pierre harbor throughout the year (COSEWIC 2007, p. 37).
    At another red knot stopover area, the Bay of Fundy, chemicals such 
as herbicides and pesticides originate from farming activities along 
tidal rivers and accumulate in intertidal areas. These contaminants 
build up in the tissues of intertidal invertebrates (e.g., the 
burrowing amphipod Corophium volutator and the small clam Macoma 
balthica) that are, in turn, ingested by shorebirds, but with unknown 
consequences (WHSRN 2012).
Contaminants--Delaware Bay
    The Delaware River and Bay biota are contaminated with PCBs and 
other pollutants (Suk and Fikslin 2006, p. 5). However, one preliminary 
study suggests that organic pollutants are not impacting shorebirds 
that eat horseshoe crab eggs. In 1992, USFWS (1996, p. i) tested 
horseshoe crab eggs, sand, and ruddy turnstones from two beaches on the 
Delaware side of Delaware Bay for organochlorines and trace metals. 
Sand, eggs, and bird tissues contained low to moderately elevated 
levels of contaminants. This limited study suggested that contamination 
of the shorebirds at Delaware Bay was probably not responsible for any 
decline in the population. However, at the time of this study, 
detection limits for organic contaminants were much higher than those 
that are now possible using current analytical capabilities. Thus, 
lower levels of contamination (which may impact wildlife) could not be 
detected by the testing that was performed (detection limits for 
horseshoe crab eggs were 0.07 to 0.20 parts per million (ppm), wet 
weight). Only one egg sample had a quantifiable level of PCBs, but this 
could have been due to the limitations of the tests to detect lower 
levels. A more extensive survey of horseshoe crab eggs throughout 
Delaware Bay would provide a more definitive assessment (USFWS 1996, p. 
i), especially if coupled with current analytical methods that can 
quantify residues at much lower concentrations. However, we are unaware 
of any plans to update this study.
    Burger et al. (1993, p. 189) examined concentrations of lead, 
cadmium, mercury, selenium, chromium, and manganese in feathers of 
shorebirds, including red knots migrating north through Cape May, New 
Jersey, in 1991 and 1992. Although these authors predicted that metal 
levels would be positively correlated with weight, this was true only 
for mercury in red knots. Selenium was negatively correlated with 
weight in red knots. No other significant correlation of metal 
concentrations with weight was found. Selenium and manganese were 
highest in red knots, while lead, mercury, chromium, and cadmium were 
higher in other species (Burger et al. 1993, p. 189). Metal levels in 
the feathers partially reflect the extent of pollution at the location 
of the birds during feather formation, so these feather concentrations 
may not necessarily correspond to exposure during the Delaware Bay 
stopover (Burger et al. 1993, p. 193). The results of this study 
suggest that the levels of cadmium, lead, mercury, selenium, and 
manganese were similar to levels reported from other shorebird studies. 
However, the levels of chromium in this study were much higher than had 
been reported for other avian species (Burger et al. 1993, pp. 195-
    Burger (1997b, p. 279) measured lead, mercury, cadmium, chromium, 
and manganese concentrations in the eggs of horseshoe crabs from 1993 
to 1995, and from leg muscle tissues in 1995, in Delaware Bay. In eggs, 
mercury levels were below 100 parts per billion (ppb), or were 
nondetectable. Cadmium levels were generally low in 1993 and 1995 but 
were relatively higher in 1994. Lead levels in eggs decreased from 558 
ppb in 1993 to 87 ppm in 1995. Selenium increased, chromium decreased, 
and manganese generally decreased. Leg muscles had significantly lower 
levels of all metals than eggs, except for mercury (Burger 1997b, p. 
279). The high levels of some metals in eggs of horseshoe crabs may 
partially account for similar high levels in the feathers of shorebirds 
that feed on crab eggs while in Delaware Bay (Burger 1997b, p. 285).
    Burger et al. (2002, p. 227) examined the levels of arsenic, 
cadmium, chromium, lead, manganese, mercury, and selenium in the eggs 
and tissues of 100 horseshoe crabs collected at 9 sites from Maine to 
Florida, including Delaware Bay. Arsenic levels were the highest, 
followed by manganese and selenium, while levels for the other metals 
averaged below 100 ppb for most tissues. The levels of contaminants

[[Page 60088]]

found in horseshoe crabs, with the possible exceptions of arsenic in 
Florida and mercury in Barnegat Bay (New Jersey) and Prime Hook 
(Delaware), were below those known to cause adverse effects in the 
crabs themselves or in organisms that consume them or their eggs.
    Revisiting the 1997 study specific to Delaware Bay, Burger et al. 
(2003, p. 36) examined the concentrations of arsenic, cadmium, 
chromium, lead, manganese, mercury, and selenium in the eggs and 
tissues of horseshoe crabs from eight locations on both sides of 
Delaware Bay. Locational differences were detected but were small. 
Further, contaminant levels were generally low. The levels of 
contaminants found in horseshoe crabs were well below those known to 
cause adverse effects in the crabs themselves or in organisms that 
consume them or their eggs. Contaminant levels have generally declined 
in the eggs of horseshoe crabs from 1993 to 2001, suggesting that 
contaminants are not likely to be a problem for secondary consumers 
like red knot, or a cause of their decline.
    Botton et al. (2006, p. 820) found no significant differences in 
the percentage of horseshoe crab eggs that completed development when 
cultured using water from Jamaica Bay (New York) or from lower Delaware 
Bay, a less polluted location. Only one percent of the embryos from 
Jamaica Bay exhibited developmental anomalies, a frequency comparable 
to a previously studied population from Delaware Bay. These authors 
suggested that the distribution and abundance of horseshoe crabs in 
Jamaica Bay were not limited by water quality (Botton et al. 2006, p. 
820). This finding suggests that horseshoe crabs are not particularly 
sensitive to differences in water quality.
    The USFWS (2007b, p. ii) examined embryonic, larval, and juvenile 
horseshoe crab responses to a series of exposures (from 0 to 100 ppb) 
of methoprene, a mosquito larvicide (a pesticide that kills specific 
insect larvae). The results provided no evidence that a treatment 
effect occurred, with no obvious acute effects of environmentally 
relevant concentrations of methoprene on developing horseshoe crab 
embryos, larvae, or first molt juveniles. The study results suggested 
that exposure to methoprene may not be a limiting factor to horseshoe 
crab populations. However, horseshoe crab life stages after the first 
molt were not tested for methoprene effects, which have been found in 
other marine arthropod species. Walker et al. (2005, pp. 118, 124) 
found that methoprene was toxic to lobster (Homarus americanus) stage 
II larvae at 1 ppb, and that stage IV larvae were more resistant but 
did exhibit significant increases in molt frequency beginning at 
exposures of 5 ppb. However, we do not have information on how or to 
what extent these levels of methoprene may affect horseshoe crab 
populations or red knots, through their consumption of exposed 
horseshoe crab eggs.
    A piping plover was found among dead shorebirds discovered on a 
sandbar near Marco Island, Florida, following the county's aerial 
application of the organophosphate pesticide Fenthion for mosquito 
control in 1997 (Pittman 2001; Williams 2001). The USEPA has 
subsequently banned the use of Fenthion (American Bird Conservancy 
2012b). Marco Island also supports an important concentration of red 
knots, but it is unknown if any red knots were affected by Fenthion at 
this or other sites.
Contaminants--South America
    Blanco et al. (2006, p. 59) documented the value of South American 
rice fields as an alternative feeding habitat for waterbirds. 
Agrochemicals are used in the management of rice fields. Although 
shorebirds are not considered harmful to the rice crop, they are 
exposed to lethal and sublethal doses of toxic products while foraging 
in these habitats. Rice fields act as important feeding areas for 
migratory shorebirds but can become toxic traps without adequate 
management (Blanco et al. 2006, p. 59). In rice field surveys from 
November 2004 to April 2005, red knots constituted only 0.7 percent of 
shorebirds observed, with three knots in Uruguay and none in Brazil or 
Argentina (Blanco et al. 2006, p. 59). Thus, exposure in these 
countries is low; however, much larger numbers of red knots (1,700) 
have been observed in rice fields in French Guiana (Niles 2012b), and 6 
red knots have been reported from rice fields in Trinidad (eBird.org 
    Threats to red knot habitat in Maranh[atilde]o, Brazil, include 
iron ore and gold mining, which can cause mercury contamination (WHSRN 
2012; Niles et al. 2008, p. 97; COSEWIC 2007, p. 37). The important 
migration stopover area at San Antonio Oeste, Argentina faces potential 
pollution from a soda ash factory built in 2005, which could release up 
to 250,000 tons of calcium chloride per year, affecting intertidal 
invertebrate food supplies. Garbage and port activities are additional 
sources of pollution in this region (WHSRN 2012; Niles et al. 2008, p. 
98; COSEWIC 2007, p. 37).
    At the southern Argentinean stopover of R[iacute]o Gallegos, a 
trash dump adjoins the feeding and roosting areas used by shorebirds. 
Garbage is spread quickly by the strong winds characteristic of the 
region and is deposited over large parts of the estuary shore. This 
trash diminishes habitat quality, especially when plastics, such as 
polythene bags, cover foraging or roosting habitats (Niles et al. 2008, 
p. 98; Ferrari et al. 2002, p. 39). Pollution at R[iacute]o Gallegos 
also stems from untreated sewage, but a project is under way to carry 
the waste offshore instead of discharging it into the shorebird 
habitats (WHSRN 2012) (see Factor A--Coastal Development--Other 
    In the past, organic waste from the City of R[iacute]o Grande (in 
Argentinean Tierra del Fuego, population approximately 50,000), 
including that from a chicken farm, has been released at high tide over 
the flats where red knots feed (Atkinson et al. 2005, p. 745). We have 
no direct evidence of red knots having been affected by organic waste, 
but it remains a potential source of contamination risk (e.g., 
nutrients, trace metals, pesticides, pathogens, pharmaceuticals, 
endocrine disruptors) (Fisher et al. 2005, pp. iii, 4, 34) to the knots 
and their wintering habitat. As at R[iacute]o Gallegos, wind-blown 
trash from a nearby landfill degrades shorebird habitats at one 
location in R[iacute]o Grande, but the City is working to relocate the 
landfill. In addition, a methanol and urea plant and two seaports are 
in development (WHSRN 2012), which could also increase pollution.
    Although red knots are exposed to a variety of contaminants across 
their nonbreeding range, we have no evidence that such exposure is 
impacting health, survival, or reproduction at the subspecies level. 
Exposure risks exist in localized red knot habitats in Canada, but best 
available data suggest shorebirds in Canada are not impacted by 
background levels of contamination. Levels of most metals in red knot 
feathers from the Delaware Bay have been somewhat high but generally 
similar to levels reported from other studies of shorebirds. One 
preliminary study suggests organochlorines and trace metals are not 
elevated in Delaware Bay shorebirds, although this finding cannot be 
confirmed without updated testing. Levels of metals in horseshoe crabs 
are generally low in the Delaware Bay

[[Page 60089]]

region and not likely impacting red knots or recovery of the crab 
    Horseshoe crab reproduction does not appear impacted by the 
mosquito control chemical methoprene (at least through the first 
juvenile molt) or by ambient water quality in mid-Atlantic estuaries. 
Shorebirds have been impacted by pesticide exposure, but use of the 
specific chemical that caused a piping plover death in Florida has 
subsequently been banned in the United States. Exposure of shorebirds 
to agricultural pollutants in rice fields may occur regionally in parts 
of South America, but red knot usage of rice field habitats was low in 
the several countries surveyed. Finally, localized urban pollution has 
been shown to impact South American red knot habitats, but we are 
unaware of any documented health effects or population-level impacts. 
Thus, we conclude that environmental contaminants are not a threat to 
the red knot. However, see Cumulative Effects, below, regarding an 
unlikely but potentially high-impact synergistic effect among avian 
influenza, environmental contaminants, and climate change in Delaware 
Factor E--Wind Energy Development
    Within the red knot's U.S. wintering and migration range, 
substantial development of offshore wind facilities is planned, and the 
number of wind turbines installed on land has increased considerably 
over the past decade. The rate of wind energy development will likely 
continue to increase into the future as the United States looks to 
decrease reliance on the traditional sources of energy (e.g., fossil 
fuels). Wind turbines can have a direct (e.g., collision mortality) and 
indirect (e.g., migration disruption, displacement from habitat) impact 
on shorebirds. We have no information on wind energy development trends 
in other countries, but risks of red knot collisions would likely be 
similar wherever large numbers of turbines are constructed along 
migratory pathways, either on land or offshore.
Wind Energy--Offshore
    In 2007, the DOI's Bureau of Ocean Energy Management (BOEM)--
formerly called the Minerals Management Service (MMS) and the Bureau of 
Ocean Energy Management, Regulation, and Enforcement (BOEMRE))--
established an Alternative Energy and Alternate Use Program for the 
U.S. OCS, under which BOEM may issue leases, easements, and rights-of-
way for the production and transmission of non-oil and -gas energy 
sources (MMS 2007, p. 2). Since 2009, DOI has developed a regulatory 
framework for offshore wind projects in Federal waters and launched an 
initiative to facilitate the siting, leasing, and construction of new 
projects (Department of Energy (DOE) and BOEMRE 2011, p. iii). In 2011, 
the U.S. Department of Energy (DOE) and BOEM released a National 
Offshore Wind Strategy (National Strategy) that articulates a national 
goal of 54 gigawatts (GW) of deployed offshore wind-generating capacity 
by 2030, with an interim target of 10 GW of capacity deployed by 2020. 
To achieve these targets, the United States would have to reduce the 
cost of offshore wind energy production and the construction timelines 
of offshore wind facilities. The National Strategy illustrates the 
commitment of DOE and DOI to spur the rapid and responsible development 
of offshore wind energy (DOE and BOEMRE 2011, p. iii).
    In addition to these Federal efforts, several States are 
considering installation of offshore wind turbines in their 
jurisdictional ocean waters (i.e., up to 3 nautical miles (5.6 km) off 
the Atlantic coast; variable distances in the Gulf of Mexico) (DOE 
2013; Rhode Island Coastal Resources Management Council 2012, p. i). 
Although New Jersey is pursuing wind projects in State waters, State 
officials concluded in 2009 that Delaware Bay is not an appropriate 
site for a large-scale wind turbine project because of potential 
impacts to shorebirds (NJDEP 2009a, p. 1; NJDEP 2009b, entire). 
Delaware has plans to document shorebird movement patterns to and from 
Delaware Bay during the stopover to identify siting locations that will 
minimize wind turbine impacts to these species (Kalasz 2008, p. 40).
    To date, no offshore wind facilities have been installed in the 
United States. However in 2010, BOEM issued the first lease to build a 
wind facility in Federal waters, authorizing the Cape Wind Energy 
Project off the southeast coast of Massachusetts (DOE and BOEMRE 2011, 
p. 41). Mapping from BOEM (2013) shows additional leases have been 
executed for two smaller areas about 10 and 16 mi (16 and 26 km) 
southeast of Atlantic City, New Jersey and for a larger area about 14 
mi (22 km) southeast of the mouth of the Delaware Bay. Offshore wind 
projects have been proposed off the coasts of Texas and Northern Mexico 
(Newstead et al. in press), and five States recently entered an 
agreement with the Federal Government to facilitate wind energy 
development in the Great Lakes (Council on Environmental Quality 2012, 
p. 1).
    Analysis by the DOE shows the potential for wind energy, and 
offshore wind in particular, to reduce greenhouse gas emissions in a 
rapid and cost[hyphen]effective manner (DOE and BOEMRE 2011, p. 5). 
However, large-scale installation of offshore wind turbines represents 
a potential collision hazard for red knots during their migration 
(Burger et al. 2012c, p. 370; Burger et al. 2011, p. 348; Watts 2010, 
p. 1), and offshore wind resources within the U.S. range of the red 
knot show high potential for wind energy development (DOE and BOEMRE 
2011, pp. 5-6). Avian collision risks are related to both the total 
number of turbines and the height of the turbines (Kuvlesky et al. 
2007, p. 2488; NRC 2007, p. 138; Chamberlain et al. 2006, p. 198). 
Increasing power output per turbine is key to reducing the cost of 
offshore wind energy generation, necessitating the development of 
larger turbines (DOE and BOEMRE 2011, p. 15). As approved, the Cape 
Wind Energy facility will include 130, 3.6-megawatt (MW) wind turbines, 
each with a maximum blade height of 440 ft (134 m) above sea level 
(BOEM 2012, p. 1). The DOE and BOEM envision the height of offshore 
turbines increasing to 617 ft (188 m) above sea level for 8-MW turbines 
by 2020, and to 681 ft (207.5 m) above sea level for 10-MW turbines by 
2030 (DOE and BOEMRE 2011, p. 15). Using a range of 3.6 to 10 MW of 
generating capacity per turbine, the national goal of 54 GW would 
require between 5,400 and 15,000 turbines to be installed in U.S. 
    Buildout (when all available sites are either developed or 
restricted) of the wind industry along the Atlantic coast will result 
in the largest network of overwater avian hazards ever constructed, 
adding a new source of mortality to many bird populations (Watts 2010, 
p. 1), some of which can little tolerate further reductions before 
realizing population-level effects. Watts (2010, p. 1) used a form of 
harvest theory called Potential Biological Removal to develop a 
population framework for estimating sustainable limits on human-induced 
bird mortality. Enough information was available from the literature 
for 46 nongame waterbird species to allow for estimates of sustainable 
mortality limits from all human-caused sources. Among these 46 
populations, red knot stood out as having particularly low mortality 
limits (Watts 2010, p. 1).
    Using an estimated rangewide population size of 20,000 red knots, 
Watts (2010, p. 39) estimated that human-induced direct mortality 
exceeding 451 birds per year would start to cause population declines. 
This estimate of 451 birds per year could

[[Page 60090]]

increase with the use of updated estimates of population size (see the 
``Population Surveys and Estimates'' section of the Rufa Red Knot 
Ecology and Abundance supplemental document) and survival (e.g., 
Schwarzer et al. 2012, p. 729; McGowan et al. 2011a, p. 13). While the 
Watts (2010, p. 39) model underscores the vulnerability of red knot 
populations to direct human-caused mortality from any source (see also 
Oil Spills and Leaks, Harmful Algal Blooms, and Factor B, above), we 
have only preliminary information on the actual red knot collision risk 
posed by offshore wind turbines (e.g., based on collision rates in 
other countries, the effects of weather and artificial lighting, 
behavioral avoidance capacity, flight altitudes, migration routes). 
Best available data regarding these risk factors are presented below, 
but are currently insufficient to estimate the likely annual mortality 
of red knots upon buildout of offshore wind infrastructure.
    Research from Europe, where several offshore wind facilities are in 
operation, suggests that bird collision rates with offshore turbines 
may be higher than for turbines on land. For various waterbird species, 
annual collision rates from 6.7 to 19.1 birds per turbine have been 
reported (Kuvlesky et al. 2007, p. 2489). Collision risks depend on 
turbine design and configuration, geography, attractiveness of the 
habitat, behavior and ecology of the species, habitat and spatial use, 
and ability of the birds to perceive and avoid wind turbines at close 
range (Burger et al. 2011, p. 340; Kuvlesky et al. 2007, p. 2488; NRC 
2007, p. 138).
    A number of studies from Europe also suggest that wind facilities 
could displace migrating waterfowl and shorebirds, create barriers to 
migration, and alter flight paths between foraging and roosting 
habitats (Kuvlesky et al. 2007, p. 2489). Such effects are thought to 
extend at least 1,969 ft (600 m) from the wind facility, but could 
extend 1.2 to 4.5 mi (2 to 4 km) for some species (Kuvlesky et al. 
2007, p. 2490). Avoidance of wind energy facilities varies among 
species and depends on site, season, tide, and whether the facility is 
in operation. Disturbance tends to be greatest for migrating birds 
while feeding and resting (NRC 2007, p. 108). As with the potential for 
increasing hurricane frequency or severity (discussed under 
Asynchronies--Fall Migration, above), extra flying to avoid obstacles 
during migration represents additional energy expenditure (Niles et al. 
2010a, p. 129), which could impact survival as well as the timing of 
arrival at stopover areas (see Asynchronies, above). However, 
displacement of birds from habitats around wind facilities somewhat 
reduces the risks of turbine collisions.
    Although little shorebird-specific information is available, the 
effect of weather on migrating bird flight altitudes has been well 
documented through the use of radar and thermal imagery. Numerous 
studies indicate that the risk of bird collisions with wind turbines 
(including offshore turbines) increases as weather conditions worsen 
and visibility decreases (Drewitt and Langston 2006, p. 31; H[uuml]ppop 
et al. 2006, pp. 102, 105-107; Exo et al. 2003 p. 51). If birds are 
migrating at high altitudes and suddenly encounter fog, precipitation, 
or strong head winds, they may be forced to fly at lower altitudes, 
increasing their collision risks if they fly in the rotor (i.e., 
turbine blade) swept zone (Drewitt and Langston 2006, p. 31). Avoidance 
behavior is likely to vary according to conditions. It is reasonable to 
expect that avoidance rates would be much reduced at times of poor 
visibility, in poor weather, at night (Chamberlain et al. 2006, p. 
199), and under varying structure illumination conditions (Drewitt and 
Langston 2006, p. 31; H[uuml]ppop et al. 2006, p. 105). The greatest 
collision risk occurs at night, particularly in unfavorable weather 
conditions. Behavioral observations have shown that most birds fly 
closer to the height of turbine rotor blades at night than during day, 
and that more birds collide with rotor blades at night than by day (Exo 
et al. 2003, p. 51).
    Burger et al. (2011, pp. 341-342) used a weight-of-evidence 
approach to examine the risks and hazards from offshore wind 
development on the OCS for three species of coastal waterbirds, 
including red knot. Three levels of exposure were identified: Micro-
scale (whether the species is likely to fly within the rotor swept 
area, governed by behavioral avoidance abilities); meso-scale 
(occurrence within the rotor swept zone or hazard zone, governed by 
flight altitude); and macro-scale (occurrence of species within the 
geographical areas of interest). Regarding micro-scale exposure, little 
is known about the red knot's abilities to behaviorally avoid turbine 
collisions (Burger et al. 2011, p. 346), an important factor in 
determining collision risk (Chamberlain et al. 2006, p. 198). The red 
knot's visual acuity and maneuverability are known to be good, but no 
actual interactions with wind turbines have been observed. The red 
knot's ability to avoid turbines, even if normally good, could be 
reduced in poor visibility, high winds, or inclement weather.
    Avoidance may be more difficult upon descent after long migratory 
flights than on ascent (Burger et al. 2011, p. 346). Lighting on tall 
structures has been shown to be a significant risk factor in avian 
collisions (Kuvlesky et al. 2007, p. 2488; Manville 2009; entire). 
Particularly during inclement weather, birds become disoriented and 
entrapped in areas of artificially lighted airspace. Although the 
response of red knots to lighting is not known, red knots are inferred 
to migrate during both night and day, based on flight durations and 
distances documented by geolocators (Normandeau Associates, Inc. 2011, 
p. 203), and lighting is generally required on wind turbines for 
aviation safety (Federal Aviation Administration 2007, pp. 33-34).
    Regarding meso-scale exposure, the migratory flight altitude of red 
knots remains unknown (Normandeau Associates, Inc. 2011, p. 203). 
However, some experts estimate the normal cruising altitude of red 
knots during migration to be in the range of 3,281 to 9,843 ft (1,000 
to 3,000 m), well above the estimated height of even a 10-MW turbine 
(681 ft; 207.5 m). However, much lower flight altitudes may be expected 
when red knots encounter bad weather or high winds, on ascent or 
descent from long-distance flights, during short-distance flights if 
they are blown off course, during short coastal migration flights, or 
during daily commuting flights (e.g., between foraging and roosting 
habitats) (Burger et al. 2012c, pp. 375-376; Burger et al. 2011, p. 
346). As judged by tree heights, Burger et al. (2012c, p. 376) observed 
knots flying at heights of up to 400 ft (120 m) when flying away from 
disturbances and when moving between foraging and roosting areas. Based 
on observations of ruddy turnstones and other Calidris canutus 
subspecies departing from Iceland towards Nearctic breeding rounds in 
spring 1986 to 1988, Alerstam et al. (1990, p. 201) found that 
departing shorebirds climbed steeply, often by circling and soaring 
flight, with an average climbing rate of 3.3 ft per second (1.0 m per 
second) up to altitudes of 1,969 to 6,562 ft (600 to 2,000 m) above sea 
level. With unfavorable winds, the shorebirds descended to fly low over 
the sea surface (Alerstam et al. 1990, p. 201).
    Regarding macro-scale exposure, red knot migratory crossings of the 
Atlantic OCS are likely to occur broadly throughout this ocean region, 
with possible concentrations south of Cape Cod in fall and south of 
Delaware Bay in spring (Normandeau Associates, Inc. 2011, p. 201). 
Shorter-distance migrants (e.g., those wintering in the Southeast)

[[Page 60091]]

were initially thought to be at lower risk of collision with offshore 
turbines, particularly turbines located far off the coast such as in 
the OCS (Burger et al. 2011, pp. 346, 348). However, information from 
nine geolocator tracks showed that both short-distance and long-
distance (e.g., birds wintering in South America) migrants crossed the 
OCS at least twice per year, with some birds crossing as many as six 
times. These numbers reflect only long flights, and many more crossings 
of the OCS may occur as red knots make shorter flights between states 
(Burger et al. 2012c, p. 374). The geolocator results suggest that 
short-distance migrants may actually face greater collision hazards 
from wind development in this region. The six birds that wintered in 
the Southeast spent an average of 218 days (60 percent of the year) 
migrating, stopping over, or wintering on the U.S. Atlantic coast, 
while the 3 birds that wintered in South America spent only about 22 
days (about 6 percent of the year) in this region (Burger et al. 2012c, 
p. 374). Thus, long-distance migrants may spend less time exposed to 
turbines built off the U.S. Atlantic coast.
    South of the Atlantic coast stopovers, red knots' migratory 
pathways may be either coast-following, OCS-crossing, or a mixture of 
both (Normandeau Associates, Inc. 2011, p. 202). While some extent of 
coast-following is likely to occur, studies to date suggest that a 
large fraction of the population is likely to cross the OCS at 
significant distances offshore (e.g., to follow direct pathways between 
widely separated migration stopover points) (Burger et al. 2012c, p. 
376; Normandeau Associates, Inc. 2011, p. 202). Based on the red knot's 
life history and geolocator results to date, macro-scale exposure of 
red knots to wind facilities is likely to be widely but thinly spread 
over the Atlantic OCS (Normandeau Associates, Inc. 2011, p. 202). 
Hazards to red knots from wind energy development likely increase for 
facilities situated closer to shore, particularly near bays and 
estuaries that serve as major stopover or wintering areas (Burger et 
al. 2011, p. 348).
    Although exposure of red knots to collisions with offshore wind 
turbines is broad geographically, exposure is much more restricted 
temporally, occurring mainly during brief portions of the spring and 
fall migration when long migratory flights occur over open water 
(Normandeau Associates, Inc. 2011, p. 202). The rest of the red knot's 
annual cycle is largely restricted to coastal and near-shore habitats 
(Normandeau Associates, Inc. 2011, p. 202), during which times 
collision hazards with land-based turbines (discussed below) would 
represent a greater hazard than for turbines in the offshore 
    Taking advantage of the limited temporal exposure of migrating 
birds to offshore turbine collisions, the authorization for one 
offshore wind facility in New Jersey's State waters includes 
operational shutdowns during certain months when red knots and two 
federally listed bird species (piping plovers and roseate terns) may be 
present. The shutdowns would occur only during inclement weather 
conditions (USFWS 2012d, p. 3) that may prompt lower migration 
altitudes and hinder avoidance behaviors.
Wind Energy--Terrestrial
    The number of land-based wind turbines installed within the U.S. 
range of the red knot has increased substantially in the past decade 
(table 13). As of 2009, estimates of total avian mortality at U.S. 
turbines ranged from 58,000 to 440,000 birds per year, and were 
associated with high uncertainty due to inconsistencies in the duration 
and intensity of monitoring studies (Manville 2009, p. 268). In 2008, 
DOE released a report to investigate the feasibility of achieving 20 
percent of U.S. electricity from wind by 2030 (DOE 2008, p. 1), a 
scenario that would substantially reduce U.S. carbon dioxide emissions 
(DOE 2008, p. 107). The 20 percent wind scenario envisions 251 GW of 
land-based generation in addition to 54 GW of shallow-water offshore 
production (DOE 2008, p. 10). Using an average capacity of 2 MW per 
turbine (University of Michigan 2012, p. 1), a 251-GW target would 
require about 125,500 turbines. The DOI strongly supports renewable 
energy, including wind development, and the Service works to ensure 
that such development is bird- and habitat-friendly (Manville 2009, p. 
268). In 2012, the Service updated the 2003 voluntary guidelines to 
provide a structured, scientific process for addressing wildlife 
conservation concerns at all stages of land-based wind energy 
development (USFWS 2012e, p. vi).

  Table 13--Installed Wind Energy Generation Capacity by State Within the U.S. Range of the Red Knot (Including
                             Interior Migration Pathways), 1999 and 2012 (DOE 2012).
 [U.S. average turbine size was 1.97 MW in 2011, up from 0.89 MW in 2000 (University of Michigan 2012, p. 1). We
           divided the megawatts by these average turbine sizes to estimate the numbers of turbines.]
                                                         1999                                2012
                                                                Estimated                           Estimated
                  State                       Megawatts         number of         Megawatts         number of
                                                                turbines                            turbines
Alabama.................................             0.000                 0                 0                 0
Arkansas................................             0.000                 0                 0                 0
Colorado................................                24            21.600             2,301             1,168
Connecticut.............................             0.000                 0                 0                 0
Delaware................................             0.000                 0                 2                 1
Florida.................................             0.000                 0                 0                 0
Georgia.................................             0.000                 0                 0                 0
Illinois................................             0.000                 0             3,568             1,811
Indiana.................................             0.000                 0             1,543               783
Iowa....................................           242.420               272             5,137             2,608
Kansas..................................             1.500                 2             2,712             1,377
Kentucky................................             0.000                 0                 0                 0
Louisiana...............................             0.000                 0                 0                 0
Maine...................................             0.100                 0               431               219
Maryland................................             0.000                 0               120                61
Massachusetts...........................             0.300                 0               100                51
Michigan................................             0.600                 1               988               502
Minnesota...............................           273.390               307             2,986             1,516
Mississippi.............................             0.000                 0                 0                 0
Missouri................................             0.000                 0               459               233

[[Page 60092]]

Montana.................................             0.100                 1               645               327
Nebraska................................             2.820                 3               459               233
New Hampshire...........................             0.050                 0               171                87
New Jersey..............................             0.000                 0                 9                 5
New York................................             0.000                 0             1,638               831
North Carolina..........................             0.000                 0                 0                 0
North Dakota............................             0.390                 1             1,679               852
Ohio....................................             0.000                 0               426               216
Oklahoma................................             0.000                 0             3,134             1,591
Pennsylvania............................             0.130                 1             1,340               680
Rhode Island............................             0.000                 0                 9                 5
South Carolina..........................             0.000                 0                 0                 0
South Dakota............................             0.000                 0               784               398
Tennessee...............................             0.000                 0                29                15
Texas...................................           183.520               206            12,212             6,199
Vermont.................................             6.050                 7               119                60
Virginia................................             0.000                 0                 0                 0
West Virginia...........................             0.000                 0               583               296
Wisconsin...............................            22.980                26               649               329
Wyoming.................................            72.515                81             1,410               716
    Total...............................           828.465               931            45,643            23,169

    Although avian impacts from land-based wind turbines are generally 
better documented than in the offshore environment, relatively little 
shorebird-specific information is available. Compiling estimated 
mortality rates from nine U.S. wind facilities (including four in 
California), Erickson et al. (2001, pp. 2, 37) calculated an average of 
2.19 avian fatalities per turbine per year for all bird species 
combined, and found that shorebirds constituted only 0.2 percent of the 
total. Compiling 18 studies around the Great Lakes from 1999 to 2009, 
Akios (2011, pp. 9-10) found that mortality estimates for all species 
combined ranged from 0.4 to nearly 14 birds per turbine per year. 
Shorebirds accounted for 4.3 percent of the total at inland sites (nine 
studies at six sites), but accounted for only about 1.5 percent of the 
total at sites closer to the lakeshores (five studies at four sites) 
(Akios 2011, p. 14). Studies from Europe and New Jersey also suggest 
generally low collision susceptibility for shorebirds at coastal wind 
turbines (Normandeau Associates, Inc. 2011, p. 201).
    Even in coastal states, most of the wind capacity installed to date 
is located along interior ridgelines or other areas away from the 
coast. With operations starting in 2005 (Atlantic County Utilities 
Authority 2012, p. 1), the 7.5-MW Jersey Atlantic Wind Farm was the 
first coastal wind farm in the United States (New Jersey Clean Energy 
Program undated). Located outside of Atlantic City, New Jersey (about 2 
mi (3.2 km) inland from the nearest sandy beach, and surrounded by 
tidal marsh), the facility consists of five 380-ft (116-m) turbines 
(Atlantic County Utilities Authority 2012, p. 1). The New Jersey 
Audubon Society (NJAS (also known as New Jersey Audubon) 2009, entire; 
NJAS 2008a, entire; NJAS 2008b, entire) reported raw data from carcass 
searches conducted around the turbines. These figures have not yet been 
adjusted for observer efficiency, scavenger removal, or lack of 
searching in restricted-access areas, all of which would increase 
estimates of collision mortality (NJAS 2009, p. 2). In 3 years of 
searching, 38 carcasses from 25 species were attributed to turbine 
collision (NJAS 2009, pp. 2-3), or about 2.5 collisions per turbine per 
year. Of these, three carcasses (about eight percent) were shorebirds, 
and none were red knots (NJAS 2009, p. 3; NJAS 2008a, p. 5; NJAS 2008b, 
p. 9).
    Considerable wind facility development has occurred in recent years 
near the Texas coast, south of Corpus Christi, and in the Mexican State 
of Tamaulipas; many additional wind energy projects are proposed in 
this region (Newstead et al. in press). As of 2011, coastal wind 
installations in Texas totaled more than 1,200 MW, or about 13 to 15 
percent of the Statewide total (Reuters 2011). Kuvlesky et al. (2007, 
pp. 2487, 2492-2493) identified the lower Gulf coast of Texas as a 
region where wind energy development may have a potentially negative 
effect on migratory birds. Onshore wind energy development in the area 
of Laguna Madre may expose red knots to direct and indirect impacts 
during daily or seasonal movements (Newstead et al. in press). 
Shorebirds departing the coast for destinations along the central 
flyway (see the ``Migration--Northwest Gulf of Mexico'' section of the 
Rufa Red Knot Ecology and Abundance supplemental document) may be at 
some risk from wind projects throughout the flyway, but especially 
those that are adjacent to the coast where birds on a northbound 
departure may not have reached sufficient altitude to clear turbine 
height before reaching migration altitude (Newstead et al. in press).
Wind Energy--Summary
    We analyzed shorebird mortality at land-based wind turbines in the 
United States, and we considered the red knot's vulnerability factors 
for collisions with offshore wind turbines that we expect will be built 
in the next few decades. We have no information regarding wind energy 
development in other countries. Based on our analysis of wind energy 
development in the United States, we expect ongoing improvements in 
turbine siting, design, and operation will help minimize bird collision 
hazards. However, we also expect cumulative avian collision mortality 
to increase

[[Page 60093]]

through 2030 as the number of turbines continues to grow, and as wind 
energy development expands into coastal and offshore environments. 
Shorebirds as a group have constituted only a small percentage of 
collisions with U.S. turbines in studies conducted to date, but wind 
development along the coasts (where shorebirds might be at greater 
risk) did not begin until 2005.
    We are not aware of any documented red knot mortalities at any wind 
turbines to date, but low levels of red knot mortality from turbine 
collisions may be occurring now based on the number of turbines along 
the red knot's migratory routes (table 13) and the frequency with which 
red knots traverse these corridors. Based on the current number and 
geographic distribution of turbines, if any such mortality is 
occurring, it is likely not causing subspecies-level effects. However, 
as buildout of offshore, coastal, and inland wind energy infrastructure 
progresses, increasing mortality from turbine collisions may contribute 
to a subspecies-level effect due to the red knot's vulnerability to 
direct human-caused mortality. We anticipate that the threat to red 
knots from wind turbines will be primarily related to collision or 
behavioral changes during migratory or daily flights. Unless facilities 
are constructed at key stopover or wintering habitats, we do not expect 
wind energy development to cause significant direct habitat loss or 
degradation or displacement of red knots from otherwise suitable 
Factor E--Conservation Efforts
    There are many components of Factor E, some of which are being 
partially managed through conservation efforts. For example, the 
reduced availability of horseshoe crab eggs from the past overharvest 
of crabs in Delaware Bay is currently being managed through the ASMFC's 
ARM framework (see Reduced Food Availability, above, and supplemental 
document--Factor D). This conservation effort more than others is 
likely having the greatest effect on the red knot subspecies as a whole 
because a large majority of the birds move through Delaware Bay during 
spring migration and depend on a superabundant supply of horseshoe crab 
eggs for refueling. Other factors potentially influencing horseshoe 
crab egg availability are outside the scope of the ARM, but some are 
being managed. For example, enforcement is ongoing to minimize 
poaching, and steps are being implemented to prevent the importation of 
nonnative horseshoe crab species that could impact native populations. 
Despite the ARM and other conservation efforts, horseshoe crab 
population growth has stagnated for unknown reasons, some of which 
(e.g., possible ecological shifts) may not be manageable. See Factor A 
regarding threats to, and conservation efforts to maintain, horseshoe 
crab spawning habitat.
    Some threats to the red knot's other prey species (mainly mollusks) 
are being partially addressed. For example, the Service is working with 
partners to minimize the effects of shoreline stabilization projects on 
the invertebrate prey base for shorebirds (e.g., Rice 2009, entire), 
and management of ORVs is protecting the invertebrate prey resource in 
some areas. Other likely threats to the red knot's mollusk prey base 
(e.g., ocean acidification; warming coastal waters; marine diseases, 
parasites, and invasive species) cannot be managed at this time, 
although efforts to minimize ballast water discharges in coastal areas 
likely reduce the potential for introduction of new invasive species.
    Other smaller-scale conservation efforts implemented to reduce 
Factor E threats include beach recreation management to reduce human 
disturbance, gull species population monitoring and management in 
Delaware Bay, research into HAB control, oil spill response plan 
development and implementation, sewage treatment in R[iacute]o Gallegos 
(Argentina), and national and state wind turbine siting and operation 
guidelines. In contrast, no known conservation actions are available to 
address asynchronies during the annual cycle.
Factor E--Summary
    Factor E includes a broad range of threats to the red knot. Reduced 
food availability at the Delaware Bay stopover site due to commercial 
harvest of the horseshoe crab is considered a primary causal factor in 
the decline of rufa red knot populations in the 2000s. Under the 
current management framework (the ARM), the present horseshoe crab 
harvest is not considered a threat to the red knot, but it is not yet 
known if the horseshoe crab egg resource will continue to adequately 
support red knot populations over the next 5 to 10 years. 
Notwithstanding the importance of the horseshoe crab and Delaware Bay, 
the red knot faces a range of ongoing and emerging threats to its food 
resources throughout its range, including small prey sizes from unknown 
causes, warming water and air temperatures, ocean acidification, 
physical habitat changes, possibly increased prevalence of disease and 
parasites, marine invasive species, and burial and crushing of 
invertebrate prey from sand placement and recreational activities.
    In addition, the red knot's life-history strategy makes this 
species inherently vulnerable to mismatches in timing between its 
annual cycle and those periods of optimal food and weather conditions 
upon which it depends. The red knot's sensitivity to timing 
asynchronies has been demonstrated through a population-level response, 
as the late arrivals of birds in Delaware Bay is generally accepted as 
a key causative factor (along with reduced supplies of horseshoe crab 
eggs) behind population declines in the 2000s. The factors that caused 
delays in the spring migrations of red knots from Argentina and Chile 
are still unknown, and we have no information to indicate if this delay 
will reverse, persist, or intensify. Superimposed on the existing 
threat of late arrivals in Delaware Bay are new threats emerging due to 
climate change, such as changes in the timing of reproduction for both 
horseshoe crabs and mollusks. Climate change may also cause shifts in 
the period of optimal arctic insect and snow conditions relative to the 
time period when red knots currently breed. The red knot's adaptive 
capacity to deal with numerous changes in the timing of resource 
availability across its geographic range is largely unknown. A few 
examples suggest some flexibility in red knot migration strategies, but 
differences between the annual timing cues of red knots (at least 
partly celestial and endogenous) and their prey (primarily 
environmental) suggest there are limitations on the adaptive capacity 
of red knots to cope with increasing frequency or severity of 
    Other threats are likely to exacerbate the effects of reduced prey 
availability and asynchronies, including human disturbance, competition 
with gulls, and behavioral changes from wind energy development. 
Additional threats are likely to increase the levels of direct red knot 
mortality, such as HABs, oil spills and other contaminants, and 
collisions with wind turbines. In addition to elevating background 
mortality rates, these three threats pose the potential for a low-
probability but high-impact event if a severe HAB or major oil or 
contaminant spill occurs when and where large numbers of red knots are 
present, or if a mass-collision event occurs at wind turbines during 
migration. Based on our review of the best scientific and commercial 
data available, the subspecies-level impacts from Factor E components 
are already occurring and are anticipated to continue and possibly 
increase into the future.

[[Page 60094]]

Cumulative Effects from Factors A through E
    Cumulative means an increase in quantity, degree, or force by 
successive addition. Synergy means the interaction of elements that, 
when combined, produce a total effect that is greater than the sum of 
the individual elements. Red knots face a wide range of threats across 
their range on multiple geographic and temporal scales. The effects of 
some smaller threats may act in an additive fashion to ultimately 
impact populations or the subspecies as a whole (cumulative effects). 
Other threats may interact synergistically to increase or decrease the 
effects of each threat relative to the effects of each threat 
considered independently (synergistic effects).
    An example of cumulative effects comes from local or regional 
sources of typically low-level but ongoing direct mortality, such as 
from hunting, normal levels of parasites and predation, stochastic 
weather events, toxic HAB events, oil pollution, and collisions with 
wind turbines. We have no evidence that any of these mortality sources 
individually are impacting red knot populations, but taken together, 
the cumulative effect of these threats may potentially aggravate 
population declines, or slow population recoveries, particularly since 
modeling has suggested that the red knot is inherently vulnerable to 
direct human-caused mortality (Watts 2010, p. 39). Red knots by nature 
flock together within wintering areas and at critical migration 
stopovers. Surveys indicate that red knot populations using Tierra del 
Fuego and Delaware Bay have decreased by about 75 percent since the 
1980s. As a result, flocks of several hundred to a thousand birds now 
represent a greater proportion of the total red knot population than in 
the past. Natural or anthropogenic stochastic events affecting these 
flocks can, therefore, be expected to have a greater impact on the red 
knot subspecies as a whole than in the past.
    An example of a localized synergistic effect is increased beach 
cleaning following a storm, HAB event, or oil spill. Red knots and 
their habitats can be impacted by both the initial event, and then 
again by the cleanup activities. Sometimes such response efforts are 
necessary to minimize the birds' exposure to toxins, but nonetheless 
cause further disturbance and possibly alter habitats (e.g., N. 
Douglass pers. comm. December 4, 2006). Where storms occur in areas 
with hard stabilization structures, they are likely to cause net losses 
of habitat. In a synergistic effect, these same storms can also trigger 
or accelerate human efforts to stabilize the shoreline, further 
affecting shorebird habitats as discussed under Factor A. In addition 
to causing direct mortality and prompting human response actions, 
storm, oil spill, or HAB events can interact synergistically with 
several other threats, for example, exacerbating ongoing problems with 
habitat degradation or food availability through physical or toxic 
effects on habitat or prey species.
    Modeling the effect of winds on migration in Calidris canutus 
canutus, Shamoun-Baranes et al. (2010, p. 285) found that unpredictable 
winds affect flight times and that wind is a predominant driver of the 
use of an intermittently used emergency stopover site. This study 
points to the interactions between weather and habitat. The somewhat 
uncertain but nevertheless likely threat to red knots from changing 
frequency, intensity, geographic paths, or timing of coastal storms 
could have a synergistic effect with loss or degradation of stopover 
habitats (e.g., changing storm patterns could intensify the red knot's 
need for a robust network of stopover sites). Likewise, encounters with 
more frequent, severe, or aberrant storms during migration might not 
only exact some direct mortality and the energetic costs (to survivors) 
of extra flight miles, but also could induce red knots to increase 
their use of stopover habitats in areas where shorebird hunting is 
still practiced (Nebel 2011, p. 217).
    Reduced food availability has also been shown to interact 
synergistically with asynchronies and several other threats. Escudero 
et al. (2012, p. 362) have suggested that declining prey quality in 
South American wintering areas may be a partial explanation for the 
increasing proportion of red knots arriving late in Delaware Bay in the 
2000s. In turn, the best available data indicate that late arrivals in 
Delaware Bay were a key factor that acted synergistically with 
depressed horseshoe crab egg supplies, and together these two factors 
constitute the most well-supported explanation for red knot population 
declines in the 2000s (Niles et al. 2008, p. 2; Atkinson et al. 2007, 
p. 892; Baker et al. 2004, p. 878; Atkinson et al. 2003b, p. 16). 
Further synergistic effects in Delaware Bay affecting red knot weight 
gain have also been noted among food availability, ambient weather, 
storms, habitat conditions, and competition with gulls (Dey et al. 
2011a, p. 7; Breese 2010, p. 3; Niles et al. 2005, p. 4). Philippart et 
al. (2003, p. 2171) concluded that prolonged periods of lowered bivalve 
recruitment and stocks due to rising water temperatures may lead to a 
reformulation of estuarine food webs and possibly a reduction of the 
resilience of the system to additional disturbances, such as shellfish 
harvest. Modeling by van Gils et al. (2005a, p. 2615) showed that, by 
selecting stopovers containing high-quality prey, Calidris canutus of 
various subspecies kept metabolic rates at a minimum, potentially 
reducing the spring migratory period by a full week; thus, not only can 
asynchronies cause red knots to arrive when food supplies are 
suboptimal, but so can suboptimal prey quality at a stopover cause an 
asynchrony for the next leg of the migratory journey (e.g., by delaying 
departure until adequate weight has been gained).
    While direct predation by peregrine falcons may account for only 
minor losses of individual birds, observations by shorebird biologists 
in Virginia, Delaware, and New Jersey have found that the presence of 
peregrine falcons significantly affects red knot foraging patterns, 
causing birds to abandon or avoid beaches that otherwise would be used 
for foraging. During times of limited food availability, this 
disturbance could reduce the proportion of red knots that can attain 
sufficient weight for successful migration and breeding in the Arctic. 
As with predation, human disturbance can also have a synergistic effect 
with reduced food availability. The combined effects of these two 
threats (food availability and disturbance) at one key wintering site 
(R[iacute]o Grande, Argentina, in Tierra del Fuego) caused the red 
knot's energy intake rate to drop from the highest known for red knots 
anywhere in the world in 2000, to among the lowest in 2008 (Escudero et 
al. 2012, pp. 359-362). Especially when food resources are limited, 
human disturbance can also exacerbate competition in Delaware Bay by 
giving a competitive advantage to gull species, which return to 
foraging more quickly than shorebirds do, following a flight response 
to vehicles, people, or dogs (Burger et al. 2007, p. 1164). Shorebirds 
can tolerate more disturbance before their fitness levels are reduced 
when feeding conditions are favorable (e.g., abundant prey, mild 
weather) (Niles et al. 2008, p. 105; Goss-Custard et al. 2006, p. 88).
    In Delaware Bay, the potential exists for an unlikely but, if it 
occurred, high-impact synergistic effect among disease, environmental 
contaminants, and climate change. Because Delaware Bay is a known 
hotspot for low pathogenicity avian influenza (LPAI) among shorebirds, 
this region may act as

[[Page 60095]]

a place where novel avian viruses (potentially including high 
pathogenicity (HP) forms) can amplify and subsequently spread in North 
America (Brown et al. 2013, p. 2). The Delaware River and Bay are also 
contaminated with PCBs (Suk and Fikslin 2006, p. 5), which are known to 
suppress the immune systems in waterbirds, such as herring gulls and 
black-crowned night herons (Nycticorax nycticorax) (Grasman et al. 2013 
pp. 548, 559). If resident Delaware Bay birds are immunosuppressed by 
PCB tissue concentrations (which is unknown but possible), the 
potential exists for resident bird species such as mallards (Anas 
platyrhynchos) (Fereidouni et al. 2009, pp. 1, 6) or herring gulls 
(Brown et al. 2008, p. 394) to more easily acquire a virulent HPAI, 
which could then be transmitted to red knots during the spring 
stopover. Health impacts and mortality from HPAI have been shown in 
Calidris canutus islandica (Reperant et al. 2011, entire) and can be 
presumed in the rufa subspecies. Such an occurrence would be likely to 
exact high mortality on red knots.
    In mallards, Fereidouni et al. (2009, pp. 1, 6) found that prior 
exposure to LPAI conferred some immunity to HPAI and could, therefore, 
increase the risk of mallards transmitting virulent forms of the 
disease (i.e., they tend to survive the HPAI and, therefore, can spread 
it). Olsen et al. (2006, p. 388) suggested that many wild bird species 
may be partially immune to HPAI due to previous exposure to LPAI, 
enhancing their potential to carry HPAI to previously unaffected areas. 
The applicability of this finding to shorebirds is unknown, but this 
finding suggests that species with high rates of LPAI (e.g. ruddy 
turnstone, mallards (Brown et al. 2013, p. 2)) could be at higher risk 
of transmitting HPAI, while red knots (with low rates of LPAI) could be 
more likely to die from HPAI, if exposed. Further, modeling has 
suggested that, if climate change leads to mismatches between the 
phenology of ruddy turnstones (the main LPAI carriers) and horseshoe 
crab spawning, the prevalence of LPAI in turnstones would be projected 
to increase even as their population size decreased (Brown and Rohani 
2012, p. 1). Although the risk of a PCB-mediated HPAI outbreak in 
Delaware Bay is currently unquantifiable, the findings of Brown and 
Rohani (2012, p. 1) suggest that this risk could be increased by 
climate change (e.g., by further increasing LPAI infection rates among 
ruddy turnstones and thereby enhancing their potential to survive and 
subsequently spread HPAI, should it occur).
    In the Arctic, synergistic interactions are expected to occur among 
shifting vegetation communities, loss of sea ice, changing 
relationships between red knots and their predators and competitors, 
and the timing of snow melt and insect emergence. Such changes are 
superimposed on the red knot's breeding season that naturally has very 
tight tolerances in time and energy budgets due to the harsh tundra 
conditions and the knot's exceptionally long migration. High 
uncertainty exists about when and how such synergistic effects may 
affect red knot survival or reproduction, but the impacts are 
potentially profound (Fraser et al. 2013, entire; Schmidt et al. 2012, 
p. 4421; Meltofte et al. 2007, p. 35; Ims and Fuglei 2005, entire; 
Piersma and Lindstr[ouml]m 2004, entire; Rehfisch and Crick 2003, 
entire; Piersma and Baker 2000, entire; Z[ouml]ckler and Lysenko 2000, 
entire; Lindstr[ouml]m and Agrell 1999, entire). For example, as 
conditions warm, vegetative conditions in the current red knot breeding 
range are likely to become increasingly dominated by trees and shrubs 
over the next century. It is unknown if red knots will respond to 
vegetative and other ecosystem changes by shifting their breeding range 
north, where they could face greater energetic demands of a longer 
migration, competition with Calidris canutus islandica, and possibly no 
reduction in predation pressure if predator densities also shift north 
as temperatures warm. Alternatively, red knots may attempt to adapt to 
changing conditions within their current breeding range, where they 
could face unfavorable vegetative conditions and a new suite of 
predators and competitors expanding northward.


    Section 4 of the Act (16 U.S.C. 1533), and its implementing 
regulations at 50 CFR part 424, set forth the procedures for adding 
species to the Federal Lists of Endangered and Threatened Wildlife and 
Plants. Under section 4(a)(1) of the Act, we may list a species based 
on (A) The present or threatened destruction, modification, or 
curtailment of its habitat or range; (B) Overutilization for 
commercial, recreational, scientific, or educational purposes; (C) 
Disease or predation; (D) The inadequacy of existing regulatory 
mechanisms; or (E) Other natural or manmade factors affecting its 
continued existence. Listing actions may be warranted based on any of 
the above threat factors, singly or in combination.
    We have carefully assessed the best scientific and commercial data 
available regarding the past, present, and future threats to the rufa 
red knot. We have identified threats to the red knot attributable to 
Factors A, B, C, and E. The primary driving threats to the red knot are 
from habitat loss and degradation due to sea level rise, shoreline 
stabilization, and Arctic warming (Factor A), and reduced food 
availability and asynchronies in the annual cycle (Factor E). Other 
threats are moderate in comparison to the primary threats; however, 
cumulatively, they could become significant when working in concert 
with the primary threats if they further reduce the species' 
resiliency. These secondary threats include hunting (Factor B); 
predation (Factor C); and human disturbance, harmful algal blooms, oil 
spills, and wind energy development (Factor E). All of these factors 
affect red knots across their current range.
    Conservation efforts are being implemented in many areas of the red 
knot's range (see Factors A, B, C, and E). For example, in 2012, the 
ASMFC adopted the ARM for the management of the horseshoe crab 
population in the Delaware Bay Region to meet the dual objectives of 
maximizing crab harvest and meeting red knot population targets (ASMFC 
2012e, p. 1). In addition, regulatory mechanisms exist that provide 
protections for the red knot directly (e.g., MBTA protections against 
take for scientific study or by hunting) or through regulation of 
activities that threaten red knot habitat (e.g., section 404 of the 
Clean Water Act, Rivers and Harbors Act, Coastal Barrier Resources Act, 
and Coastal Zone Management Act, and State regulation of shoreline 
stabilization and coastal development) (see supplemental document--
Factor D). While these conservation efforts and existing regulatory 
mechanisms reduce some threats to the red knot, significant risks to 
the subspecies remain.
    Red knots migrate annually between their breeding grounds in the 
Canadian Arctic and several wintering regions, including the Southeast 
United States, the Northeast Gulf of Mexico, northern Brazil, and 
Tierra del Fuego at the southern tip of South America. During both the 
spring and fall migrations, red knots use key staging and stopover 
areas to rest and feed. This life-history strategy makes this species 
inherently vulnerable to numerous changes in the timing of quality food 
and habitat resource availability across its geographic range. While a 
few examples suggest the species has some flexibility in migration 
strategies, the full scope of

[[Page 60096]]

the species' adaptability to changes in its annual cycle is unknown.
    The Act defines an endangered species as any species that is ``in 
danger of extinction throughout all or a significant portion of its 
range'' and a threatened species as any species ``that is likely to 
become endangered throughout all or a significant portion of its range 
within the foreseeable future.'' We find that the rufa red knot meets 
the definition of a threatened species due to the likelihood of habitat 
loss driven by climate change and human response to climate change and 
reduced food resources and further asynchronies in its annual cycle 
that result in the species' reduced redundancy, resiliency, and 
representation. While there is uncertainty as to how long it may take 
some of the climate-induced changes to manifest in population-level 
effects to the rufa red knot, we find that the best available data 
suggests the rufa red knot is not at a high risk of a significant 
decline in the near term. However, should the reduction in redundancy, 
resiliency, and representation culminate in an abrupt and large loss, 
or initiation of a steep rate of decline, of reproductive capability or 
we subsequently find that the species does not have the adaptive 
capacity to adjust to actual shifts in its food and habitat resources, 
then the red knot would be at higher risk of a significant decline in 
the near term, and thus would meet the definition of an endangered 
species under the Act. We base this determination on the immediacy, 
severity, and scope of the threats described above. Therefore, on the 
basis of the best available scientific and commercial data, we propose 
listing the rufa red knot as a threatened species in accordance with 
sections 3(6) and 4(a)(1) of the Act.
    Under the Act and our implementing regulations, a species may 
warrant listing if it meets the definition of an endangered or 
threatened species throughout all or a significant portion of its 
range. The rufa red knot proposed for listing in this rule is wide-
ranging and the threats occur throughout its range. Therefore, we 
assessed the status of the subspecies throughout its entire range. The 
threats to the survival of the subspecies are not restricted to any 
particular significant portion of that range. Accordingly, our 
assessment and proposed determination applies to the subspecies 
throughout its entire range.

Available Conservation Measures

    Conservation measures provided to species listed as endangered or 
threatened under the Act include recognition, recovery actions, 
requirements for Federal protection, and prohibitions against certain 
practices. Recognition through listing results in public awareness and 
conservation by Federal, State, Tribal, and local agencies, private 
organizations, and individuals. The Act encourages cooperation with the 
States and requires that recovery actions be carried out for all listed 
species. The protection required by Federal agencies and the 
prohibitions against certain activities are discussed, in part, below.
    The primary purpose of the Act is the conservation of endangered 
and threatened species and the ecosystems upon which they depend. The 
ultimate goal of such conservation efforts is the recovery of these 
listed species, so that they no longer need the protective measures of 
the Act. Subsection 4(f) of the Act requires the Service to develop and 
implement recovery plans for the conservation of endangered and 
threatened species. The recovery planning process involves the 
identification of actions that are necessary to halt or reverse the 
species' decline by addressing the threats to its survival and 
recovery. The goal of this process is to restore listed species to a 
point where they are secure, self-sustaining, and functioning 
components of their ecosystems.
    Recovery planning includes the development of a recovery outline 
shortly after a species is listed and preparation of a draft and final 
recovery plan. The recovery outline guides the immediate implementation 
of urgent recovery actions and describes the process to be used to 
develop a recovery plan. Revisions of the plan may be done to address 
continuing or new threats to the species, as new substantive 
information becomes available. The recovery plan identifies site-
specific management actions that set a trigger for review of the five 
factors that control whether a species remains endangered or may be 
downlisted or delisted, and methods for monitoring recovery progress. 
Recovery plans also establish a framework for agencies to coordinate 
their recovery efforts and provide estimates of the cost of 
implementing recovery tasks. Recovery teams (composed of species 
experts, Federal and State agencies, nongovernmental organizations, and 
stakeholders) are often established to develop recovery plans. When 
completed, the recovery outline, draft recovery plan, and final 
recovery plan will be available on our Web site (http://www.fws.gov/endangered), or from our New Jersey Fish and Wildlife Office (see FOR 
    Implementation of recovery actions generally requires the 
participation of a broad range of partners, including other Federal 
agencies, States, Tribes, nongovernmental organizations, businesses, 
and private landowners. Examples of recovery actions include habitat 
restoration (e.g., restoration of native vegetation), research, captive 
propagation and reintroduction, and outreach and education. The 
recovery of many listed species cannot be accomplished solely on 
Federal lands because their ranges may occur primarily or solely on 
non-Federal lands. Recovery of these species requires cooperative 
conservation efforts on private, State, and Tribal lands.
    If this species is listed, funding for recovery actions will be 
available from a variety of sources, including Federal budgets, State 
programs, and cost-share grants for non-Federal landowners, the 
academic community, and nongovernmental organizations. In addition, 
pursuant to section 6 of the Act, States regularly inhabited by rufa 
red knots during the wintering or stopover periods would be eligible 
for Federal funds to implement management actions that promote the 
protection or recovery of the rufa red knot. Information on our grant 
programs that are available to aid species recovery can be found at: 
    Although the rufa red knot is only proposed for listing under the 
Act at this time, please let us know if you are interested in 
participating in recovery efforts for this species. Additionally, we 
invite you to submit any new information on this species whenever it 
becomes available and any information you may have for recovery 
planning purposes (see FOR FURTHER INFORMATION CONTACT).
    Section 7(a) of the Act requires Federal agencies to evaluate their 
actions with respect to any species that is proposed or listed as an 
endangered or threatened species and with respect to its critical 
habitat, if any is designated. Regulations implementing this 
interagency cooperation provision of the Act are codified at 50 CFR 
part 402. Section 7(a)(4) of the Act requires Federal agencies to 
confer with the Service on any action that is likely to jeopardize the 
continued existence of a species proposed for listing or result in 
destruction or adverse modification of proposed critical habitat. If a 
species is listed subsequently, section 7(a)(2) of the Act requires 
Federal agencies to ensure that activities they authorize, fund, or 
carry out are not likely to jeopardize the continued existence of the 
species or destroy or adversely

[[Page 60097]]

modify its critical habitat. If a Federal action may affect a listed 
species or its critical habitat, the responsible Federal agency must 
enter into formal consultation with the Service.
    Federal agency actions within the species habitat that may require 
conference or consultation or both as described in the preceding 
paragraph include management and landscape altering activities on 
Federal lands administered by the Department of Defense, the Service, 
and NPS; issuance of section 404 Clean Water Act permits and shoreline 
stabilization projects implemented by the USACE; construction and 
management of gas pipeline rights-of-way by the Federal Energy 
Regulatory Commission; leasing of Federal waters by the BOEM for the 
construction of wind turbines; and construction and maintenance of 
roads or highways by the Federal Highway Administration.
    The Act and its implementing regulations set forth a series of 
general prohibitions and exceptions that apply to all endangered 
wildlife. The prohibitions of section 9(a)(2) of the Act, codified at 
50 CFR 17.21 for endangered wildlife, in part, make it illegal for any 
person subject to the jurisdiction of the United States to take 
(includes harass, harm, pursue, hunt, shoot, wound, kill, trap, 
capture, or collect; or to attempt any of these), import, export, ship 
in interstate commerce in the course of commercial activity, or sell or 
offer for sale in interstate or foreign commerce any listed species. 
Under the Lacey Act (18 U.S.C. 42-43; 16 U.S.C. 3371-3378), it is also 
illegal to possess, sell, deliver, carry, transport, or ship any such 
wildlife that has been taken illegally. Certain exceptions apply to 
agents of the Service and State conservation agencies.
    We may issue permits to carry out otherwise prohibited activities 
involving endangered and threatened wildlife species under certain 
circumstances. Regulations governing permits are codified at 50 CFR 
17.22 for endangered species, and at 17.32 for threatened species. With 
regard to endangered wildlife, a permit must be issued for the 
following purposes: For scientific purposes, to enhance the propagation 
or survival of the species, and for incidental take in connection with 
otherwise lawful activities.
    Our policy, as published in the Federal Register on July 1, 1994 
(59 FR 34272), is to identify to the maximum extent practicable at the 
time a species is listed, those activities that would or would not 
constitute a violation of section 9 of the Act. The intent of this 
policy is to increase public awareness of the potential effect of a 
listing on proposed and ongoing activities within the range of species 
proposed for listing. The following activities could potentially result 
in a violation of section 9 of the Act; this list is not comprehensive:
    (1) Unauthorized collecting, handling, possessing, selling, 
delivering, carrying, or transporting of the species, including import 
or export across State lines and international boundaries, except for 
properly documented antique specimens of these taxa at least 100 years 
old, as defined by section 10(h)(1) of the Act;
    (2) Introduction of nonnative species that compete with or prey 
upon the rufa red knot, or that cause declines of the red knot's prey 
    (3) Unauthorized modification of intertidal habitat that regularly 
support concentrations of rufa red knots during the wintering or 
stopover periods; and
    (4) Unauthorized discharge of chemicals or fill material into any 
waters along which the rufa red knot is known to occur.
    (1) The following activities are not likely to result in a 
violation of section 9 of the Act; this list is not comprehensive: 
Harvest of horseshoe crabs in accordance with the ARM, provided the ARM 
is implemented as intended (e.g., including implementation of necessary 
monitoring programs), and enforced.
    Questions regarding whether specific activities would constitute a 
violation of section 9 of the Act should be directed to the New Jersey 
Fish and Wildlife Office (see FOR FURTHER INFORMATION CONTACT). 
Requests for copies of the regulations concerning listed animals and 
general inquiries regarding prohibitions and permits may be addressed 
to the U.S. Fish and Wildlife Service, Endangered Species Permits, 300 
Westgate Center Drive, Hadley, MA, 01035 (telephone 413-253-8615; 
facsimile 413-253-8482).
    Under section 4(d) of the Act, the Secretary has discretion to 
issue such regulations as he deems necessary and advisable to provide 
for the conservation of threatened species. Our implementing 
regulations (50 CFR 17.31) for threatened wildlife generally 
incorporate the prohibitions of section 9 of the Act for endangered 
wildlife, except when a ``special rule'' promulgated pursuant to 
section 4(d) of the Act has been issued with respect to a particular 
threatened species. In such a case, the general prohibitions in 50 CFR 
17.31 would not apply to that species, and instead, the special rule 
would define the specific take prohibitions and exceptions that would 
apply for that particular threatened species, which we consider 
necessary and advisable to conserve the species. The Secretary also has 
the discretion to prohibit by regulation with respect to a threatened 
species any act prohibited by section 9(a)(1) of the Act. Exercising 
this discretion, which has been delegated to the Service by the 
Secretary, the Service has developed general prohibitions that are 
appropriate for most threatened species in 50 CFR 17.31 and exceptions 
to those prohibitions in 50 CFR 17.32. We are not proposing to 
promulgate a special section 4(d) rule, and as a result, all of the 
section 9 prohibitions, including the ``take'' prohibitions, will apply 
to the rufa red knot. (As described above, harvest of horseshoe crabs 
in accordance with the ARM is not likely to result in take under 
section 9 of the Act.)
    Listing the rufa red knot under the Act would invoke provisions 
under various State laws that would prohibit take and encourage 
conservation by State government agencies. Further, States may enter 
into agreements with Federal agencies to administer and manage areas 
required for the conservation, management, enhancement, or protection 
of endangered species. Funds for these activities could be made 
available under section 6 of the Act (Cooperation with the States). 
Thus, the Federal protection afforded to these species by listing them 
as endangered species will be reinforced and supplemented by protection 
under State law.
    A determination to list the rufa red knot as a threatened species 
under the Act, if we ultimately determine that listing is warranted, 
will not regulate greenhouse gas emissions. Rather, it will reflect a 
determination that the rufa red knot meets the definition of a 
threatened species under the Act, thereby establishing certain 
protections for it under the Act. While we acknowledge that listing 
will not have a direct impact on those aspects of climate change 
impacting the rufa red knot (e.g., sea level rise, ocean acidification, 
warming coastal waters, changing patterns of coastal storm activity, 
warming of the Arctic), we expect that listing will indirectly enhance 
national and international cooperation and coordination of conservation 
efforts, enhance research programs, and encourage the development of 
mitigation measures that could help slow habitat loss and population 
declines. In addition, the development of a recovery plan will guide 
efforts intended to ensure the long-term survival and eventual recovery 
of the rufa red knot.

[[Page 60098]]

Required Determinations

Clarity of the Rule

    We are required by Executive Orders 12866 and 12988 and by the 
Presidential Memorandum of June 1, 1998, to write all rules in plain 
language. This means that each rule we publish must:
    (1) Be logically organized;
    (2) Use the active voice to address readers directly;
    (3) Use clear language rather than jargon;
    (4) Be divided into short sections and sentences; and
    (5) Use lists and tables wherever possible.
    If you feel that we have not met these requirements, send us 
comments by one of the methods listed in the ADDRESSES section. To 
better help us revise the rule, your comments should be as specific as 
possible. For example, you should tell us the numbers of the sections 
or paragraphs that are unclearly written, which sections or sentences 
are too long, the sections where you feel lists or tables would be 
useful, etc.

National Environmental Policy Act (42 U.S.C. 4321 et seq.)

    We have determined that environmental assessments and environmental 
impact statements, as defined under the authority of the National 
Environmental Policy Act of 1969, need not be prepared in connection 
with listing a species as an endangered or threatened species under the 
Endangered Species Act. We published a notice outlining our reasons for 
this determination in the Federal Register on October 25, 1983 (48 FR 

References Cited

    A complete list of all references cited in this proposed rule is 
available on the Internet at http://www.regulations.gov or upon request 
from the Field Supervisor, New Jersey Field Office (see FOR FURTHER 


    The primary authors of this proposed rule are the staff members of 
the New Jersey Field Office (see FOR FURTHER INFORMATION CONTACT).

List of Subjects in 50 CFR Part 17

    Endangered and threatened species, Exports, Imports, Reporting and 
recordkeeping requirements, and Transportation.

Proposed Regulation Promulgation

    Accordingly, we propose to amend part 17, subchapter B of chapter 
I, title 50 of the Code of Federal Regulations, as set forth below:


1. The authority citation for part 17 continues to read as follows:

    Authority: 16 U.S.C. 1361-1407; 1531-1544; 4201-4245; unless 
otherwise noted.
2. In Sec.  17.11(h) add an entry for ``Knot, rufa red'' to the List of 
Endangered and Threatened Wildlife in alphabetical order under Birds to 
read as set forth below:

Sec.  17.11  Endangered and threatened wildlife.

* * * * *
    (h) * * *

                        Species                                                      Vertebrate
--------------------------------------------------------                          population where                       When      Critical     Special
                                                             Historic range        endangered  or         Status        listed      habitat      rules
           Common name                Scientific name                                threatened
                                                                      * * * * * * *
                                                                      * * * * * * *
Knot, rufa red...................  Calidris canutus      Argentina, Aruba,      Entire..............  T               ..........         N/A         N/A
                                    ssp. rufa.            Bahamas, Barbados,
                                                          Belize, Brazil,
                                                          British Virgin
                                                          Islands, Canada,
                                                          Cayman Islands,
                                                          Chile, Colombia,
                                                          Costa Rica, Cuba,
                                                          Dominican Republic,
                                                          El Salvador, France
                                                          (Guadeloupe, French
                                                          Guiana), Guatemala,
                                                          Guyana, Haiti,
                                                          Jamaica, Mexico,
                                                          Panama, Paraguay,
                                                          Suriname, Trinidad
                                                          and Tobago, Uruguay,
                                                          Venezuela, U.S.A.
                                                          (AL, AR, CT, CO, DE,
                                                          FL, GA, IA, IL, IN,
                                                          KS, KY, LA, MA, MD,
                                                          ME, MI, MN, MO, MS,
                                                          MT, NE, NC, ND, NH,
                                                          NJ, NY, OH, OK, PA,
                                                          RI, SC, SD, TN, TX,
                                                          VA, VT, WI, WV, WY,
                                                          Puerto Rico, U.S.
                                                          Virgin Islands).
                                                                      * * * * * * *

    Dated: September 6, 2013.
Rowan W. Gould,
Acting Director, U.S. Fish and Wildlife Service.
[FR Doc. 2013-22700 Filed 9-27-13; 8:45 am]