[Federal Register Volume 78, Number 132 (Wednesday, July 10, 2013)]
[Proposed Rules]
[Pages 41499-41547]
From the Federal Register Online via the Government Printing Office [www.gpo.gov]
[FR Doc No: 2013-16521]
[[Page 41499]]
Vol. 78
Wednesday,
No. 132
July 10, 2013
Part II
Department of the Interior
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Fish and Wildlife Service
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50 CFR Part 17
Endangered and Threatened Wildlife and Plants; Threatened Status for
the Northern Mexican Gartersnake and Narrow-headed Gartersnake;
Proposed Rule
Federal Register / Vol. 78 , No. 132 / Wednesday, July 10, 2013 /
Proposed Rules
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DEPARTMENT OF THE INTERIOR
Fish and Wildlife Service
50 CFR Part 17
[Docket No. FWS-R2-ES-2013-0071; 4500030113]
RIN 1018-AY23
Endangered and Threatened Wildlife and Plants; Threatened Status
for the Northern Mexican Gartersnake and Narrow-headed Gartersnake
AGENCY: Fish and Wildlife Service, Interior.
ACTION: Proposed rule.
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SUMMARY: We, the U.S. Fish and Wildlife Service (Service), propose to
list the northern Mexican gartersnake (Thamnophis eques megalops) and
narrow-headed gartersnake (Thamnophis rufipunctatus) as 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 these species. The effect of this regulation is to
conserve northern Mexican and narrow-headed gartersnakes under the Act.
DATES: We will accept comments received or postmarked on or before
September 9, 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 August 26, 2013.
ADDRESSES: You may submit comments by one of the following methods:
(1) Electronically: Go to the Federal eRulemaking Portal: http://www.regulations.gov. Search for Docket No. FWS-R2-ES-2013-0071, which
is the docket number for this rulemaking. When you locate this
document, 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-R2-ES-2013-0071; Division of Policy and
Directives Management; U.S. Fish and Wildlife Service; 4401 N. Fairfax
Drive, MS 2042-PDM; Arlington, VA 22203.
We request that you send comments only by the methods described
above. We will post all comments on http://www.regulations.gov. This
generally means that we will post any personal information you provide
us (see the Information Requested section below for more information).
FOR FURTHER INFORMATION CONTACT: Steve Spangle, Field Supervisor, U.S.
Fish and Wildlife Service, Arizona Ecological Services Field Office,
2321 West Royal Palm Road, Suite 103, Phoenix, AZ 85021; telephone:
602-242-0210; facsimile: 602-242-2513. If you use a telecommunications
device for the deaf (TDD), call the Federal Information Relay Service
(FIRS) at 800-877-8339.
SUPPLEMENTARY INFORMATION:
Executive Summary
Why we need to publish a rule. Under the Endangered Species Act
(Act), if a species is determined to be an endangered or threatened
species 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 one year. Listing a species
as an endangered or threatened species can only be completed by issuing
a rule. Elsewhere in today's Federal Register, we propose to designate
critical habitat for the northern Mexican and narrow-headed
gartersnakes under the Act.
This document consists of:
A proposed rule to list the northern Mexican and narrow-
headed gartersnakes as threatened species throughout their ranges, and
A proposed special rule under section 4(d) under the Act
that outlines the prohibitions necessary and advisable for the
conservation of the northern Mexican gartersnake.
The basis for our action. Under the Act, we can 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. In the case of the northern Mexican and narrow-
headed gartersnakes, we have determined that harmful nonnative species
(spiny-rayed fish, bullfrogs, and crayfish), wildfires, and land uses
that divert, dry up, or significantly pollute aquatic habitat have
solely or collectively affected these gartersnakes, and several of
their native prey species, such that their resiliency, redundancy, and
representation across their ranges have been significantly compromised.
We will seek peer review. We are seeking comments from
knowledgeable individuals with scientific expertise to review our
analysis of the best available science and application of that science
and to provide any additional scientific information to improve this
proposed rule. Because we will consider all comments and information
received during the comment period, our final determinations may differ
from this proposal.
Information Requested
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 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 species' biology, range, and population trends, including:
(a) 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 these species, their
habitat or both.
(2) The factors that are the basis for making a listing
determination for these species under section 4(a) of the Act (16
U.S.C. 1531 et seq.), which are:
(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.
(3) Biological, commercial trade, or other relevant data concerning
any threats (or lack thereof) to these species and existing regulations
that may be addressing those threats.
(4) Additional information concerning the historical and current
status, range, distribution, and population size of these species,
including the locations of any additional populations of these species.
(5) Any information on the biological or ecological requirements of
these species, and ongoing conservation measures for the species and
their habitats.
(6) Any information on the projected and reasonably likely impacts
of climate
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change on the northern Mexican gartersnake and narrow-headed
gartersnake.
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 a threatened or endangered
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
section.
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, Arizona Ecological Services Field Office (see FOR
FURTHER INFORMATION CONTACT).
Previous Federal Actions
The northern Mexican and narrow-headed gartersnakes were placed on
the list of candidate species as Category 2 species on September 18,
1985 (50 FR 37958). Category 2 species were those for which existing
information indicated that listing was possibly appropriate, but for
which substantial supporting biological data to prepare a proposed rule
were lacking. In the 1996 Candidate Notice of Review (February 28,
1996; 61 FR 7596), the use of Category 2 candidates was discontinued,
and the northern Mexican and narrow-headed gartersnakes were no longer
recognized as candidates.
On December 19, 2003, we received a petition from the Center for
Biological Diversity (``petitioner'') dated December 15, 2003,
requesting that we list the northern Mexican gartersnake as threatened
or endangered, and that we designate critical habitat concurrently with
the listing. The petition was clearly identified as a petition for a
listing rule and contained the names, signatures, and addresses of the
requesting parties. Included in the petition was supporting information
regarding the species' taxonomy and ecology, historical and current
distribution, present status, and actual and potential causes of
decline. We acknowledged the receipt of the petition in a letter to the
petitioner, dated March 1, 2004. In that letter, we also advised that,
due to funding constraints in fiscal year (FY) 2004, we would not be
able to begin processing the petition at that time.
On May 17, 2005, the petitioner filed a complaint for declaratory
and injunctive relief, challenging our failure to issue a 90-day
finding for the northern Mexican gartersnake in response to the
petition as required by 16 U.S.C. 1533(b)(3)(A) and (B). In a
stipulated settlement agreement, we agreed to submit a 90-day finding
to the Federal Register by December 16, 2005, and if substantial,
submit a 12-month finding to the Federal Register by September 15, 2006
(Center for Biological Diversity v. Norton, CV-05-341-TUC-CKJ (D. Az)).
The settlement agreement was signed and adopted by the District Court
of Arizona on August 2, 2005.
On December 13, 2005, we made our 90-day finding that the petition
presented substantial scientific information indicating that listing
the northern Mexican gartersnake may be warranted; the finding and our
initiation of a status review was published in the Federal Register on
January 4, 2006 (71 FR 315).
On September 26, 2006, we published a 12-month finding that listing
of the northern Mexican gartersnake was not warranted because we
determined that not enough information on the subspecies' status and
threats in Mexico was known at that time (71 FR 56227). On November 17,
2007, the petitioner filed a complaint for declaratory and injunctive
relief pursuant to section 11 of the Act (16 U.S.C. 1540), seeking to
set aside the 12-month finding. Additionally, a formal opinion was
issued by the Solicitor of the Department of the Interior, ``The
Meaning of In Danger of Extinction Throughout All or a Significant
Portion of Its Range'' (U.S. DOI 2007), which provides further guidance
on how to conduct a detailed analysis of whether a species is in danger
of extinction throughout a significant portion of its range. In
December 2007, the Service withdrew the September 26, 2006, 12-month
finding in order to consider the new ``Significant Portion of the
Range'' policy. In a stipulated settlement agreement with the
petitioner, we agreed to submit a new 12-month finding to the Federal
Register by November 17, 2008 (Center for Biological Diversity v.
Kempthorne, CV-07-596-TUC-RCCJ (D. Az)). The settlement agreement was
signed and adopted by the District Court of Arizona on June 18, 2008.
On May 28, 2008, we published notice (73 FR 30596) of our intent to
initiate a status review for the northern Mexican gartersnake and
solicited the public for information on the status of, and potential
threats to, this species.
On November 25, 2008, we published a second 12-month finding that
listing of the northern Mexican gartersnake was warranted but precluded
by other listing priorities at that time (73 FR 71788). The petitioner
described three potentially listable entities of northern Mexican
gartersnake for consideration by the Service: (1) Listing the U.S.
population as a distinct population segment (DPS); (2) listing the
subspecies throughout its range in the United States and Mexico based
on its rangewide status; or (3) listing the subspecies throughout its
range in the United States and Mexico based on its status in the United
States. Because we found that listing the northern Mexican gartersnake
rangewide was warranted, there was no need to conduct any further
analysis of the remaining two options, which are smaller geographic
entities and are subsumed by the rangewide listing.
Status Assessments for Northern Mexican and Narrow-headed Gartersnakes
Background
Northern Mexican Gartersnake
Subspecies Description
The northern Mexican gartersnake ranges in color from olive to
olive-brown or olive-gray with three lighter-colored stripes that run
the length of the body, the middle of which darkens towards the tail.
It may occur with other native gartersnake species and can be difficult
for people without specific expertise to identify. The snake may reach
a maximum known length of 44 inches (in) (112 centimeters (cm)). The
pale yellow to light-tan lateral (side of
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body) stripes distinguish the northern Mexican gartersnake from other
sympatric (co-occurring) gartersnake species because a portion of the
lateral stripe is found on the fourth scale row, while it is confined
to lower scale rows for other species. Paired black spots extend along
the olive dorsolateral fields (region adjacent to the top of the
snake's back) and the olive-gray ventrolateral fields (region adjacent
to the area of the snake's body in contact with the ground). The scales
are keeled (possessing a ridge down the center of each scale). A more
detailed subspecies description can be found in our September 26, 2006
(71 FR 56227), or November 25, 2008 (73 FR 71788) 12-month findings for
this subspecies, or by reviewing Rosen and Schwalbe (1988, p. 4),
Rossman et al. (1996, pp. 171-172), Ernst and Ernst (2003, pp. 391-
392), or Manjarrez and Garcia (1993, pp. 1-5).
Taxonomy
The northern Mexican gartersnake is a member of the family
Colubridae and subfamily Natricinae (harmless live-bearing snakes)
(Lawson et al. 2005, p. 596). The taxonomy of the genus Thamnophis has
a complex history, partly because many of the species are similar in
appearance and arrangement of scales, but also because many of the
early museum specimens were in such poor and faded condition that it
was difficult to study them (Conant 2003, p. 6).
Prior to 2003, Thamnophis eques was considered to have three
subspecies, T. e. eques, T. e. megalops, and T. e. virgatenuis (Rossman
et al. 1996, p. 175). In 2003, an additional seven new subspecies were
identified under T. eques: (1) T. e. cuitzeoensis; (2) T. e.
patzcuaroensis; (3) T. e. insperatus; (4) T. e. obscurus; (5) T. e.
diluvialis; (6) T. e. carmenensis; and (7) T. e. scotti (Conant 2003,
p. 3). Common names were not provided, so in this proposed rule, we use
the scientific name for all subspecies of Mexican gartersnake other
than the northern Mexican gartersnake. These seven new subspecies were
described based on morphological differences in coloration and pattern;
have highly restricted distributions; and occur in isolated wetland
habitats within the mountainous Transvolcanic Belt region of southern
Mexico, which contains the highest elevations in the country (Conant
2003, pp. 7-8). The validity of the current taxonomy of the 10
subspecies of T. eques is accepted within the scientific community. A
more detailed description of the taxonomy of the northern Mexican
gartersnake is found in our September 26, 2006 (71 FR 56227) and
November 25, 2008 (73 FR 71788) 12-month findings for this subspecies.
Additional information regarding this subspecies' taxonomy can be found
in de Queiroz et al. (2002, p. 323), de Queiroz and Lawson (1994, p.
217), Rossman et al. (1996, pp. xvii-xviii, 171-175), Rosen and
Schwalbe (1988, pp. 2-3), Liner (1994, p. 107), and Crother et al.
(2012, p. 70).
Habitat and Natural History
Throughout its rangewide distribution, the northern Mexican
gartersnake occurs at elevations from 130 to 8,497 feet (ft) (40 to
2,590 meters (m)) (Rossman et al. 1996, p. 172) and is considered a
``terrestrial-aquatic generalist'' by Drummond and Marc[iacute]as-
Garc[iacute]a (1983, pp. 24-26). The northern Mexican gartersnake is a
riparian obligate (restricted to riparian areas when not engaged in
dispersal behavior) and occurs chiefly in the following general habitat
types: (1) Source-area wetlands (e.g., cienegas (mid-elevation wetlands
with highly organic, reducing (basic or alkaline) soils), or stock
tanks (small earthen impoundment)); (2) large-river riparian woodlands
and forests; and (3) streamside gallery forests (as defined by well-
developed broadleaf deciduous riparian forests with limited, if any,
herbaceous ground cover or dense grass) (Hendrickson and Minckley 1984,
p. 131; Rosen and Schwalbe 1988, pp. 14-16). Emmons and Nowak (2013, p.
14) found this subspecies most commonly in protected backwaters,
braided side channels and beaver ponds, isolated pools near the river
mainstem, and edges of dense emergent vegetation that offered cover and
foraging opportunities when surveying in the upper Verde River region.
Additional information on the habitat requirements of the northern
Mexican gartersnake within the United States and Mexico can be found in
our 2006 (71 FR 56227) and 2008 (73 FR 71788) 12-month findings for
this subspecies and in Rosen and Schwalbe (1988, pp. 14-16), Rossman et
al. (1996, p. 176), McCranie and Wilson (1987, pp. 11-17), Ernst and
Ernst (2003, p. 392), and Cirett-Galan (1996, p. 156).
The northern Mexican gartersnake is surface active at ambient (air)
temperatures ranging from 71 degrees Fahrenheit ([deg]F) to 91 [deg]F
(22 degrees Celsius ([deg]C) to 33 [deg]C) and forages along the banks
of waterbodies (Rosen 1991, p. 305, Table 2). Rosen (1991, pp. 308-309)
found that northern Mexican gartersnakes spent approximately 60 percent
of their time moving, 13 percent of their time basking on vegetation,
18 percent of their time basking on the ground, and 9 percent of their
time under surface cover; body temperatures ranged from 75 to 91 [deg]F
(24 to 33 [deg]C) and averaged 82 [deg]F (28 [deg]C), which is lower
than other, similar species with comparable habitat and prey
preferences. Rosen (1991, p. 310) suggested that lower preferred body
temperatures exhibited by northern Mexican gartersnakes may be due to:
(1) Their tendency to occupy cienega-like habitat, where warm air
temperatures are relatively unavailable; and (2) their tendency to
remain in dense cover. In the northern-most part of its range, the
northern Mexican gartersnake appears to be most active during July and
August, followed by June and September.
The northern Mexican gartersnake is an active predator and is
believed to heavily depend upon a native prey base (Rosen and Schwalbe
1988, pp. 18, 20). Northern Mexican gartersnakes forage along vegetated
banklines, searching for prey in water and on land, using different
strategies (Alfaro 2002, p. 209). Generally, its diet consists of
amphibians and fishes, such as adult and larval (tadpoles) native
leopard frogs (e.g., lowland leopard frog (Lithobates yavapaiensis) and
Chiricahua leopard frog (Lithobates chiricahuensis)), as well as
juvenile and adult native fish species (e.g., Gila topminnow
(Poeciliopsis occidentalis occidentalis), desert pupfish (Cyprinodon
macularius), Gila chub (Gila intermedia), and roundtail chub (Gila
robusta)) (Rosen and Schwalbe 1988, p. 18). Drummond and
Marc[iacute]as-Garc[iacute]a (1983, pp. 25, 30) found that as a
subspecies, Mexican gartersnakes fed primarily on frogs. Auxiliary prey
items may also include young Woodhouse's toads (Anaxyrus woodhousei),
treefrogs (Family Hylidae), earthworms, deermice (Peromyscus spp.),
lizards of the genera Aspidoscelis and Sceloporus, larval tiger
salamanders (Ambystoma tigrinum), and leeches (Gregory et al. 1980, pp.
87, 90-92; Rosen and Schwalbe 1988, p. 20; Holm and Lowe 1995, pp. 30-
31; Degenhardt et al. 1996, p. 318; Rossman et al. 1996, p. 176;
Manjarrez 1998, p. 465). In situations where native prey species are
rare or absent, this snake's diet may include nonnative species,
including larval and juvenile bullfrogs (Lithobates catesbeianus),
mosquitofish (Gambusia affinis) (Holycross et al. 2006, p. 23; Emmons
and Nowak 2013, p. 5), or other soft-rayed fish species. Chinese
mystery snails (Cipangopaludina chinensis) have been reported as a prey
item for northern Mexican gartersnakes at the Page Springs and Bubbling
Ponds State Fish
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Hatcheries in Arizona, but some predation attempts on snails have
proven fatal for gartersnakes because of their lower jaw becoming
permanently lodged in the snails' shell (Young and Boyarski 2012, p.
498). Venegas-Barrera and Manjarrez (2001, p. 187) reported the first
observation of a snake in the natural diet of any species of Thamnophis
after documenting the consumption by a Mexican gartersnake (subspecies
not provided) of a Mexican alpine blotched gartersnake (Thamnophis
scalaris).
Marc[iacute]as-Garc[iacute]a and Drummond (1988, pp. 129-134)
sampled the stomach contents of Mexican gartersnakes and the prey
populations at (ephemeral) Lake Tecocomulco, Hidalgo, Mexico. Field
observations indicated, with high statistical significance, that larger
Mexican gartersnakes fed primarily upon aquatic vertebrates (fishes,
frogs, and larval salamanders) and leeches, whereas smaller Mexican
gartersnakes fed primarily upon earthworms and leeches (Marc[iacute]as-
Garc[iacute]a and Drummond 1988, p. 131). Marc[iacute]as-Garc[iacute]a
and Drummond (1988, p. 130) also found that the birth of newborn T.
eques tended to coincide with the annual peak density of annelids
(earthworms and leeches). There is also preliminary evidence that birth
may coincide with a pronounced influx of available prey in a given
area, especially with that of explosive breeders, such as toads, but
more research is needed to confirm such a relationship (Boyarski 2012,
pers. comm.). Positive correlations were also made with respect to
capture rates (which are correlated with population size) of T. eques
to lake levels and to prey scarcity; that is, when lake levels were low
and prey species scarce, Mexican gartersnake capture rates declined
(Marc[iacute]as-Garc[iacute]a and Drummond 1988, p. 132). This
indicates the importance of available water and an adequate prey base
to maintaining viable populations of Mexican gartersnakes.
Marc[iacute]as-Garc[iacute]a and Drummond (1988, p. 133) found that
while certain prey items were positively associated with size classes
of snakes, the largest of specimens consume any prey available.
Native predators of the northern Mexican gartersnake include birds
of prey, other snakes (kingsnakes (Lampropeltis sp.), whipsnakes
(Coluber sp.), regal ring-necked snakes (Diadophis punctatus regalis),
etc.), wading birds, mergansers (Mergus merganser), belted kingfishers
(Megaceryle alcyon), raccoons (Procyon lotor), skunks (Mephitis sp.),
and coyotes (Canis latrans) (Rosen and Schwalbe 1988, pp. 18, 39;
Brennan et al. 2009, p. 123). Historically, large, highly predatory
native fish species such as Colorado pikeminnow may have preyed upon
northern Mexican gartersnake where the subspecies co-occurred. Native
chubs (Gila sp.) may also prey on neonatal gartersnakes.
Parasites have been observed in northern Mexican gartersnakes.
Boyarski (2008b, pp. 5-6) recorded several snakes within the population
at the Page Springs and Bubbling Ponds fish hatcheries with interior
bumps or bulges along the anterior one-third of the body. The cause of
these bumps was not identified or speculated upon, nor were there any
signs of trauma to the body of these snakes in the affected areas. Dr.
Jim Jarchow, a veterinarian with herpetological expertise, reviewed
photographs of affected specimens and suggested the bumps may likely
contain plerocercoid larvae of a pseudophyllidean tapeworm (possibly
Spirometra spp.), which are common in fish- and frog-eating
gartersnakes. This may not be detrimental to their health, provided the
bumps do not grow large enough to impair movement or other bodily
functions (Boyarski 2008b, p. 8). However, G[uacute]zman (2008, p. 102)
documented the first observation of mortality of a Mexican gartersnake
from a larval Eustrongylides sp. (endoparasitic nematode) which
``raises the possibility that infection of Mexican gartersnakes by
Eustrongylides sp. larvae might cause mortality in some wild
populations,'' especially if those populations are under stress as a
result of the presence of other threats.
Sexual maturity in northern Mexican gartersnakes occurs at 2 years
of age in males and at 2 to 3 years of age in females (Rosen and
Schwalbe 1988, pp. 16-17). Northern Mexican gartersnakes are viviparous
(bringing forth living young rather than eggs). Mating has been
documented in April and May followed by the live birth of between 7 and
38 newborns (average is 13.6) in July and August (Rosen and Schwalbe
1988, p. 16; Nowak and Boyarski 2012, pp. 351-352). However, field
observations in Arizona provide preliminary evidence that mating may
also occur during the fall, but further research is required to confirm
this hypothesis (Boyarski 2012, pers. comm.). Unlike other gartersnake
species, which typically breed annually, one study suggests that only
half of the sexually mature females within a population of northern
Mexican gartersnake might reproduce in any one season (Rosen and
Schwalbe 1988, p. 17).
Historical Distribution
Within the United States, the northern Mexican gartersnake
historically occurred predominantly in Arizona at elevations ranging
from 130 to 6,150 ft (40 to 1,875 m). It was generally found where
water was relatively permanent and supported suitable habitat. The
northern Mexican gartersnake historically occurred in every county and
nearly every subbasin within Arizona, from several perennial or
intermittent creeks, streams, and rivers as well as lentic (still, non-
flowing water) wetlands such as cienegas, ponds, or stock tanks.
Northern Mexican gartersnake records exist within the following
subbasins in Arizona: Colorado River, Bill Williams River, Agua Fria
River, Salt River, Tonto Creek, Verde River, Santa Cruz River, Cienega
Creek, San Pedro River, Babocomari River, and the Rio San Bernardino
(Black Draw) (Woodin 1950, p. 40; Nickerson and Mays 1970, p. 503;
Bradley 1986, p. 67; Rosen and Schwalbe 1988, Appendix I; 1995, p. 452;
1997, pp. 16-17; Holm and Lowe 1995, pp. 27-35; Sredl et al. 1995b, p.
2; 2000, p. 9; Rosen et al. 2001, Appendix I; Holycross et al. 2006,
pp. 1-2, 15-51; Brennan and Holycross 2006, p. 123; Radke 2006, pers.
comm.; Rosen 2006, pers. comm.; Holycross 2006, pers. comm.; Cotton et
al. 2013, p. 111). Numerous records for the northern Mexican
gartersnake (through 1996) in Arizona are maintained in the Arizona
Game and Fish Department's (AGFD) Heritage Database (1996a).
Historically, the northern Mexican gartersnake had a limited
distribution in New Mexico that consisted of scattered locations
throughout the Upper Gila River watershed in Grant and western Hidalgo
Counties, including the Upper Gila River, Mule Creek in the San
Francisco River subbasin, and the Mimbres River (Price 1980, p. 39;
Fitzgerald 1986, Table 2; Degenhardt et al. 1996, p. 317; Holycross et
al. 2006, pp. 1-2).
One record for the northern Mexican gartersnake exists for the
State of Nevada, opposite Fort Mohave, in Clark County along the shore
of the Colorado River that was dated 1911 (De Queiroz and Smith 1996,
p. 155). The subspecies may have occurred historically in the lower
Colorado River region of California, although we were unable to verify
any museum records for California. Any populations of northern Mexican
gartersnakes that may have historically occurred in either Nevada or
California were likely associated directly with the Colorado River, and
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we believe them to be currently extirpated.
Within Mexico, northern Mexican gartersnakes historically occurred
within the Sierra Madre Occidental and the Mexican Plateau in the
Mexican states of Sonora, Chihuahua, Durango, Coahuila, Zacatecas,
Guanajuato, Nayarit, Hidalgo, Jalisco, San Luis Potos[iacute],
Aguascalientes, Tlaxacala, Puebla, M[eacute]xico, Veracruz, and
Quer[eacute]taro, comprising approximately 85 percent of the total
rangewide distribution of the subspecies (Conant 1963, p. 473; 1974,
pp. 469-470; Van Devender and Lowe 1977, p. 47; McCranie and Wilson
1987, p. 15; Rossman et al. 1996, p. 173; Lemos-Espinal et al. 2004, p.
83). We are not aware of any systematic, rangewide survey effort for
the northern Mexican gartersnake in Mexico and have not found survey
data for the subspecies in Mexico to be published in the scientific
literature or otherwise readily available, outside of the information
already obtained. Therefore, we use other, tightly correlated
ecological surrogates (such as native freshwater fish) to inform
discussion on the status of aquatic communities and aquatic habitat in
Mexico, and therefore on the likely status of northern Mexican
gartersnake populations. This discussion is found below in the
subheadings pertinent to Mexico.
Current Distribution and Population Status
Where northern Mexican gartersnakes are locally abundant, they are
usually reliably detected with significantly less effort than
populations characterized as having low densities. Northern Mexican
gartersnakes are well-camouflaged, secretive, and very difficult to
detect in structurally complex, dense habitat where they could occur at
very low population densities, which characterizes most occupied sites.
Water clarity can also affect survey accuracy. We considered factors
such as the date of the last known records for northern Mexican
gartersnakes in an area, as well as records of one or more native prey
species in making a conclusion on occupancy of the subspecies. We used
the year 1980 to qualify occupancy because the 1980s marked the first
systematic survey efforts for northern Mexican gartersnakes across
their range (see Rosen and Schwalbe (1988, entire) and Fitzgerald
(1986, entire)) and the last, previous records were often dated several
decades prior and may not accurately represent the likelihood for
current occupation. Several areas where northern Mexican gartersnakes
were known to occur have received no, or very little, survey effort in
the past several decades. Variability in survey design and effort makes
it difficult to compare population sizes or trends among sites and
between sampling periods. For each of the sites discussed in Appendix A
(available at http://www.regulations.gov under Docket No. FWS-R2-ES-
2013-0071), we have attempted to translate and quantify search and
capture efforts into comparable units (i.e., person-search hours and
trap-hours) and have conservatively interpreted those results. Because
the presence of suitable prey species in an area may provide evidence
that the northern Mexican gartersnake may still persist in low density
where survey data are sparse, a record of a native prey species was
considered in our determination of occupancy of this subspecies.
Data on population status of northern Mexican gartersnakes in the
United States are largely summarized in gray literature provided
through agency reports and related documents. In our literature review
efforts that resulted in our 2006 and 2008 12-month findings (71 FR
56227 and 73 FR 71788, respectively), we found that the status of the
northern Mexican gartersnake has declined significantly in the last 30
years. We found that, in as much as 90 percent of the northern Mexican
gartersnakes' historical distribution in the United States, the
subspecies occurs at low to very low population densities or may even
be extirpated. The decline of the northern Mexican gartersnake is
primarily the result of predation by and competition with harmful
nonnative species, such as spiny-rayed fish, bullfrogs, and crayfish,
that have been intentionally released, accidentally released, or
dispersed through natural mechanisms. Regardless of how they got into
the wild, harmful nonnative species are now virtually ubiquitous
throughout the range of the northern Mexican gartersnake. Land uses
that result in the dewatering of habitat, combined with increasing
drought, have destroyed significant amounts of habitat throughout the
northern Mexican gartersnake's range and have also contributed to
population declines.
Holycross et al. (2006, p. 66) detected the northern Mexican
gartersnake at only 2 of 11 historical localities along the northern-
most part of its range from which the subspecies was previously known.
The only viable northern Mexican gartersnake populations in the United
States where the subspecies remains reliably detected are all located
in Arizona: (1) The Page Springs and Bubbling Ponds State Fish
Hatcheries along Oak Creek, (2) lower Tonto Creek, (3) the upper Santa
Cruz River in the San Rafael Valley, (4) the Bill Williams River, and
(5) the upper Verde River. In New Mexico, the northern Mexican
gartersnake may occur in extremely low population densities within its
historical distribution; limited survey effort is inconclusive to
determine extirpation. The status of the northern Mexican gartersnake
on tribal lands, such as those owned by the White Mountain or San
Carlos Apache Tribes, is poorly known due to historically limited
survey access. As stated previously, less is known specifically about
the current distribution of the northern Mexican gartersnake in Mexico
due to limited access to information on survey efforts and field data
from Mexico.
In Table 1 below, we summarize the population status of northern
Mexican gartersnakes at all known localities throughout their United
States distribution, as supported by museum records or reliable
observations. For a detailed discussion that explains the rationale for
site-by-site conclusions on occupancy, please see Appendix A (available
at http://www.regulations.gov under Docket No. FWS-R2-ES-2013-0071).
General rationale is provided in the introductory paragraph to this
section, ``Current Distribution and Population Status.''
Table 1--Current Population Status of the Northern Mexican Gartersnake in the United States. References Cited Are Provided in Appendix A
--------------------------------------------------------------------------------------------------------------------------------------------------------
Suitable physical Native prey species Harmful nonnative
Location Last record habitat present present species present Population status
--------------------------------------------------------------------------------------------------------------------------------------------------------
Gila River (NM, AZ)........... 2002.................. Yes.................. Yes.................. Yes.................. Likely not viable.
Spring Canyon (NM)............ 1937.................. Yes.................. Possible............. Likely............... Likely extirpated.
Mule Creek (NM)............... 1983.................. Yes.................. Yes.................. Yes.................. Likely not viable.
[[Page 41505]]
Mimbres River (NM)............ Likely early 1900s.... Yes.................. Yes.................. Yes.................. Likely extirpated.
Lower Colorado River (AZ)..... 1904.................. Yes.................. Yes.................. Yes.................. Likely extirpated.
Bill Williams River (AZ)...... 2012.................. Yes.................. Yes.................. Yes.................. Likely viable.
Agua Fria River (AZ).......... 1986.................. Yes.................. Yes.................. Yes.................. Likely not viable.
Little Ash Creek (AZ)......... 1984.................. Yes.................. Yes.................. Yes.................. Likely not viable.
Lower Salt River (AZ)......... 1964.................. Yes.................. Yes.................. Yes.................. Likely extirpated.
Black River (AZ).............. 1982.................. Yes.................. Yes.................. Yes.................. Likely not viable.
Big Bonito Creek (AZ)......... 1986.................. Yes.................. Yes.................. Yes.................. Likely not viable.
Tonto Creek (AZ).............. 2005.................. Yes.................. Yes.................. Yes.................. Likely viable.
Upper Verde River (AZ)........ 2012.................. Yes.................. Yes.................. Yes.................. Likely viable.
Oak Creek (AZ) (Page Springs 2012.................. Yes.................. Yes.................. Yes.................. Likely viable.
and Bubbling Ponds State Fish
Hatcheries).
Spring Creek (AZ)............. 1986.................. Yes.................. Yes.................. Yes.................. Likely not viable.
Sycamore Creek (AZ)........... 1954.................. Yes.................. Possible............. Yes.................. Likely extirpated.
Upper Santa Cruz River/San 2012.................. Yes.................. Yes.................. Yes.................. Likely viable.
Rafael Valley (AZ).
Redrock Canyon (AZ)........... 2008.................. Yes.................. Yes.................. Yes.................. Likely not viable.
Sonoita Creek (AZ)............ 1974.................. Yes.................. Possible............. Yes.................. Likely extirpated.
Scotia Canyon (AZ)............ 2009.................. Yes.................. Yes.................. No................... Likely not viable.
Parker Canyon (AZ)............ 1986.................. Yes.................. Possible............. Yes.................. Likely not viable.
Las Cienegas National 2012.................. Yes.................. Yes.................. Possible............. Likely not viable.
Conservation Area and Cienega
Creek Natural Preserve (AZ).
Lower Santa Cruz River (AZ)... 1956.................. Yes.................. Yes.................. Yes.................. Likely extirpated.
Buenos Aires National Wildlife 2000.................. Yes.................. Yes.................. Yes.................. Likely not viable.
Refuge (AZ).
Bear Creek (AZ)............... 1987.................. Yes.................. Yes.................. Yes.................. Likely not viable.
San Pedro River (AZ).......... 1996.................. Yes.................. Yes.................. Yes.................. Likely not viable.
Babocomari River and Cienega 1986.................. Yes.................. Possible............. Yes.................. Likely not viable.
(AZ).
Canelo Hills-Sonoita 2012.................. Yes.................. Yes.................. Yes.................. Likely not viable.
Grasslands Area (AZ).
San Bernardino National 1997.................. Yes.................. Yes.................. Yes.................. Likely not viable.
Wildlife Refuge (AZ).
--------------------------------------------------------------------------------------------------------------------------------------------------------
Notes: ``Possible'' means there were no conclusive data found. ``Likely extirpated'' means the last record for an area pre-dated 1980 and existing
threats suggest the species is likely extirpated. ``Likely not viable'' means the last record for an area pre-dated 1980 and existing threats suggest
the species is likely extirpated. ``Likely viable'' means that the species is reliably found with minimal to moderate survey effort and the population
is generally considered viable.
Table 1 lists the 29 known localities for the northern Mexican
gartersnake in the United States. Appendix A (available at http://www.regulations.gov under Docket No. FWS-R2-ES-2013-0071) discusses
such considerations as the physical condition of habitat, the
composition of the aquatic biological community, the existence of
significant threats, and the length of time since the last known
observation of the subspecies in presenting rationale for determining
occupancy status at each locality. We have concluded that in as many as
24 of 29 known localities in the United States (83 percent), the
northern Mexican gartersnake population is likely not viable and may
exist at low population densities that could be threatened with
extirpation or may already be extirpated. In most localities where the
species may occur at low population densities, existing survey data are
insufficient to prove extirpation. Only five populations of northern
Mexican gartersnakes in the United States are considered likely viable
where the species remains reliably detected. When considering the total
number of stream miles in the United States that historically supported
the northern Mexican gartersnake that are now permanently dewatered
(except in the case of temporary flows in response to heavy
precipitation), we concluded that as much as 90 percent of historical
populations in the United States either occur at low densities or are
extirpated. As displayed in Table 1, harmful nonnative species are a
concern in almost every northern Mexican gartersnake locality in the
United States and the most significant reason for their decline, as
discussed in depth in our threats analysis below.
Listed as threatened throughout its range in Mexico by the Mexican
Government, our understanding of the northern Mexican gartersnake's
specific population status throughout its range in Mexico is less
precise than that known for its United States distribution because
survey efforts are less, and sufficient, available records do not exist
or are difficult to obtain. However, we have assembled and reviewed an
extensive body of scientific information on known, regional threats to
northern Mexican gartersnakes and to their primary prey species. This
information is presented in greater detail below in our specific
discussion of threats to the species in Mexico.
Narrow-Headed Gartersnake
Species Description
The narrow-headed gartersnake is a small to medium-sized
gartersnake with a maximum total length of 44 in (112 cm mm) (Painter
and Hibbitts 1996, p. 147). Its eyes are set high on its unusually
elongated head, which narrows to the snout, and it lacks striping on
the dorsum (top) and sides, which distinguishes its appearance from
other gartersnake species with which it could co-occur (Rosen and
Schwalbe 1988, p. 7). The base color is usually tan or grey-brown (but
may darken) with conspicuous brown, black, or reddish spots that become
indistinct towards the
[[Page 41506]]
tail (Rosen and Schwalbe 1988, p. 7; Boundy 1994, p. 126). The scales
are keeled. Degenhardt et al. (1996, p. 327), Rossman et al. (1996, pp.
242-244), and Ernst and Ernst (2003, p. 416) further describe the
species.
Taxonomy
The narrow-headed gartersnake is a member of the family Colubridae
and subfamily Natricinae (harmless live-bearing snakes) (Lawson et al.
2005, p. 596). The taxonomy of the genus Thamnophis has a complex
history partly because many of the species are similar in appearance
and scutelation (arrangement of scales), but also because many of the
early museum specimens were in such poor and faded condition that it
was difficult to study them (Conant 2003, p. 6). The narrow-headed
gartersnake has a particularly complex taxonomic history due to its
morphology and feeding habits. There are approximately 30 species
described in the gartersnake genus Thamnophis (Rossman et al. 1996, pp.
xvii-xviii). Two large overlapping clades (related taxonomic groups) of
gartersnakes have been identified called the ``Mexican'' and
``widespread'' clades, supported by allozyme and mitochondrial DNA
genetic analyses (de Queiroz et al. 2002, p. 321). Thamnophis
rufipunctatus is a member of the ``Mexican'' clade and is most closely
related taxonomically to the southern Durango spotted gartersnake
(Thamnophis nigronuchalis) (de Queiroz and Lawson 1994, p. 217; de
Queiroz et al. 2002; p. 321).
Due to the narrow-headed gartersnake's morphology and feeding
habits, there has been considerable deliberation among taxonomists
about the correct association of this species within seven various
genera over time (Rosen and Schwalbe 1988, pp. 5-6); chiefly, between
the genera Thamnophis (the ``gartersnakes'') and Nerodia (the
``watersnakes'') (Pierce 2007, p. 5). Chaisson and Lowe (1989, pp. 110-
118) argued that the pattern of ultrastructural (as revealed by an
electron microscope) pores in the scales of narrow-headed gartersnakes
provided evidence that the species is more appropriately placed within
the genus Nerodia. However, De Queiroz and Lawson (1994, p. 217)
rejected this premise using mitochondrial DNA (mtDNA) genetic analyses
to refute the inclusion of the narrow-headed gartersnake in the genus
Nerodia and maintain the species within the genus Thamnophis.
The narrow-headed gartersnake was first described as Chilopoma
rufipunctatum by E. D. Cope (in Yarrow, 1875). Recently, Thamnophis
rufipunctatus nigronuchalis and T. r. unilabialis were recognized as
subspecies under T. rufipunctatus and comprised what was considered the
T. rufipunctatus complex. However, Rossman et al. (1996, pp. 244-246)
elevated T. r. nigronuchalis to full species designation and argued
recognition of T. r. unilabialis be discontinued due to the diagnostic
differences being too difficult to discern. Wood et al. (2011, p. 14)
used genetic analysis of the T. rufipunctatus complex to propose the
elevation of these three formerly recognized subspecies as three
distinct species, as a result of a combination of interglacial warming,
ecological and life-history constraints, and genetic drift, which
promoted differentiation of these three species throughout the warming
and cooling periods of the Pleistocene epoch (Wood et al. 2011, p. 15).
We use these most recent and complete data in acknowledging these three
entities as unique species: T. rufipunctatus (along the Mogollon Rim of
Arizona and New Mexico), T. unilabialis (Chihuahua, eastern Sonora, and
northern Durango, Mexico), and T. nigronuchalis (southern Durango,
Mexico).
Several common names have been used for this species including the
red-spotted gartersnake, the brown-spotted gartersnake, and the
currently used, narrow-headed gartersnake (Rosen and Schwalbe 1988, p.
5). Further discussion of the taxonomic history of the narrow-headed
gartersnake is available in Crother (2012, p. 71), Degenhardt et al.
(1996, p. 326); Rossman et al. (1996, p. 244), De Queiroz and Lawson
(1994, pp. 213-229); Rosen and Schwalbe (1988, pp. 5-7); and De Queiroz
et al. (2002, p. 321).
Habitat and Natural History
The narrow-headed gartersnake is widely considered to be one of the
most aquatic of the gartersnakes (Drummond and Marcias Garcia 1983, pp.
24, 27; Rossman et al. 1996, p. 246). This species is strongly
associated with clear, rocky streams, using predominantly pool and
riffle habitat that includes cobbles and boulders (Rosen and Schwalbe
1988, pp. 33-34; Degenhardt et al. 1996, p. 327; Rossman et al. 1996,
p. 246; Ernst and Ernst 2003, p. 417). Rossman et al. (1996, p. 246)
also note the species has been observed using lake shoreline habitat in
New Mexico. Narrow-headed gartersnakes occur at elevations from
approximately 2,300 to 8,200 ft (700 to 2,500 m), inhabiting Petran
Montane Conifer Forest, Great Basin Conifer Woodland, Interior
Chaparral, and the Arizona Upland subdivision of Sonoran Desertscrub
communities (Rosen and Schwalbe 1988, p. 33; Brennan and Holycross
2006, p. 122). An extensive evaluation of habitat use of narrow-headed
gartersnakes along Oak Creek in Arizona is provided in Nowak and
Santana-Bendix (2002, pp. 26-37). Rosen and Schwalbe (1988, p. 35)
found narrow-headed gartersnake densities may be highest at the
conjunction of cascading riffles with pools, where waters were deeper
than 20 in (0.5 m) in the riffle and deeper than 40 in (1 m) in the
immediately adjoining area of the pool, but more than twice the number
of snakes were found in pools rather than riffles.
Where narrow-headed gartersnakes are typically found in the water,
little aquatic vegetation exists (Rosen and Schwalbe 1988, p. 34).
However, bank-line vegetation is an important component to suitable
habitat for this species. Narrow-headed gartersnakes will usually bask
in situations where a quick escape can be made, whether that is into
the water or under substrate such as rocks (Fleharty 1967, p. 16).
Common plant species associations include Arizona alder (Alnus
oblongifolia) (highest correlation with occurrence of the narrow-headed
gartersnake), velvet ash (Fraxinus pennsylvanica), willows (Salix
ssp.), canyon grape (Vitis arizonica), blackberry (Rubus ssp.), Arizona
sycamore (Platanus wrightii), Arizona black walnut (Juglans major),
Freemont cottonwood (Populus fremontii), Gambel oak (Quercus gambelii),
and ponderosa pine (Pinus ponderosa) (Rosen and Schwalbe 1988, pp. 34-
35). Rosen and Schwalbe (1988, p. 35) noted that the composition of
bank-side plant species and canopy structure were less important to the
species' needs than was the size class of the plant species present;
narrow-headed gartersnakes prefer to use shrub- and sapling-sized
plants for thermoregulating (basking) at the waters' edge (Degenhardt
et al. 1996, p. 327).
Narrow-headed gartersnakes may opportunistically forage within
dammed reservoirs formed by streams that are occupied habitat, such as
at Wall Lake (located at the confluence of Taylor Creek, Hoyt Creek,
and the East Fork Gila River) (Fleharty 1967, p. 207) and most recently
at Snow Lake in 2012 (located near the confluence of Snow Creek and the
Middle Fork Gila River) (Hellekson 2012b, pers. comm.) in New Mexico,
but records from impoundments are rare in the literature. The species
evolved in the absence of such habitat, and impoundments are generally
managed as sport fisheries (Wall Lake and Snow Lake are) and
[[Page 41507]]
often maintain populations of harmful nonnative species that are
incompatible with narrow-headed gartersnakes.
The narrow-headed gartersnake is surface-active generally between
March and November (Nowak 2006, p. 16). Little information on suitable
temperatures for surface activity of the narrow-headed gartersnake
exists; however, it is presumed to be rather cold-tolerant based on its
natural history and foraging behavior that often involves clear, cold
streams at higher elevations. Along Oak Creek in Arizona, Nowak (2006,
Appendix 1) found the species to be active in air temperatures ranging
from 52 to 89[emsp14][deg]F (11 to 32 [deg]C) and water temperatures
ranging from 54 to 72[emsp14][deg]F (12 to 22 [deg]C). Jennings and
Christman (2011, pp. 12-14) found body temperatures of narrow-headed
gartersnakes along the Tularosa River averaged approximately
68[emsp14][deg]F (20 [deg]C) during the mid-morning hours and
81[emsp14][deg]F (27 [deg]C) in the late afternoon during the period
from late July and August. Variables that affect their body temperature
include the temperature of the microhabitat used and water temperature
(most predictive), but slope aspect and the surface area of cover used
also influenced body temperatures (Jennings and Christman 2011, p. 13).
Narrow-headed gartersnakes have a lower preferred temperature for
activity as compared to other species of gartersnakes (Fleharty 1967,
p. 228), which may facilitate their highly aquatic nature in cold
streams.
Narrow-headed gartersnakes specialize on fish as their primary prey
item (Rosen and Schwalbe 1988, p. 38; Degenhardt et al. 1996, p. 328;
Rossman et al. 1996, p. 247; Nowak and Santana-Bendix 2002, pp. 24-25;
Nowak 2006, p. 22) and are believed to be mainly visual hunters
(Hibbitts and Fitzgerald 2005, p. 364), heavily dependent on visual
cues when foraging based on comparative analyses among other species of
gartersnakes (de Queiroz 2003, p. 381). Unlike many other species of
gartersnakes that are active predators (actively crawl about in search
of prey), narrow-headed gartersnakes are considered to be ambush
predators (sit-and-wait method) (Brennan and Holycross 2006, p. 122;
Pierce et al. 2007, p. 8). The specific gravity (ratio of the mass of a
solid object to the mass of the same volume of water) of the narrow-
headed gartersnake was found to be nearly 1, which means that the snake
can maintain its desired position in the water column with ease, an
adaptation to facilitate foraging on the bottom of streams (Fleharty
1967, pp. 218-219). Native fish species most often associated as prey
items for the narrow-headed gartersnake include Sonora sucker
(Catostomus insignis), desert sucker (C. clarki), speckled dace
(Rhinichthys osculus), roundtail chub (Gila robusta), Gila chub (Gila
intermedia), and headwater chub (Gila nigra) (Rosen and Schwalbe 1988,
p. 39; Degenhardt et al. 1996, p. 328). Nonnative species used as prey
by narrow-headed gartersnakes are most often salmonid species (trout);
most commonly brown (Salmo trutta) and rainbow trout (Oncorhynchus
mykiss), as these species are commonly stocked in, or near, occupied
narrow-headed gartersnake habitat (Rosen and Schwalbe 1988, p. 39;
Nowak 2006, pp. 22-23). Fleharty (1967, p. 223) reported narrow-headed
gartersnakes eating green sunfish, but green sunfish is not considered
a suitable prey item.
Several reviews (Stebbins 1985, p. 199; Deganhardt et al. 1996, p.
328; Ernst and Ernst 2003, p. 418) state that the narrow-headed
gartersnake will also prey upon frogs, tadpoles, and salamanders.
Fitzgerald (1986, p. 6) referenced the Stebbins (1985) account as the
only substantiated account of the species accepting something other
than fish as prey, apparently as the result of finding a small
salamander larvae in the stomach of an individual in Durango, Mexico.
Formerly recognized as a subspecies of Thamnophis rufipunctatus, that
individual is now recognized as T. unilabialis (Wood et al. 2011, p.
3). We found an account of narrow-headed gartersnakes consuming red-
spotted toads in captivity (Woodin 1950, p. 40). Despite several
studies focusing on the ecology of narrow-headed gartersnakes in recent
times, there are no other records of narrow-headed gartersnakes, under
current taxonomic recognition, feeding on prey items other than fish.
We, along with species experts, do not consider amphibians as
ecologically important prey for this species based on our review of the
literature.
Native predators of the narrow-headed gartersnake include birds of
prey, other snakes such as kingsnakes, whipsnakes, or regal ring-necked
snakes, wading birds, mergansers, belted kingfishers, raccoons, skunks,
and coyotes (Rosen and Schwalbe 1988, pp. 18, 39; Brennan et al. 2009,
p. 123). Historically, large, highly predatory native fish species such
as Colorado pikeminnow may have preyed upon narrow-headed gartersnakes
where the species co-occurred. Native chubs (Gila sp.) may also prey on
neonatal gartersnakes.
Sexual maturity in narrow-headed gartersnakes occurs at 2.5 years
of age in males and at 2 years of age in females (Deganhardt et al.
1996, p. 328). Narrow-headed gartersnakes are viviparous. The
reproductive cycle for narrow-headed gartersnakes appears to be longer
than other gartersnake species; females begin the development of
follicles in early March, and gestation takes longer (Rosen and
Schwalbe 1988, pp. 36-37). Female narrow-headed gartersnakes breed
annually and give birth to 4 to 17 offspring from late July into early
August, perhaps earlier at lower elevations (Rosen and Schwalbe 1988,
pp. 35-37). Sex ratios in narrow-headed gartersnake populations can be
skewed in favor of females (Fleharty 1967, p. 212).
Historical Distribution
The historical distribution of the narrow-headed gartersnake ranged
across the Mogollon Rim and along its associated perennial drainages
from central and eastern Arizona, southeast to southwestern New Mexico
at elevations ranging from 2,300 to 8,000 ft (700 to 2,430 m) (Rosen
and Schwalbe 1988, p. 34; Rossman et al. 1996, p. 242; Holycross et al.
2006, p. 3). The species was historically distributed in headwater
streams of the Gila River subbasin that drain the Mogollon Rim and
White Mountains in Arizona, and the Gila Wilderness in New Mexico;
major subbasins in its historical distribution included the Salt and
Verde River subbasins in Arizona, and the San Francisco and Gila River
subbasins in New Mexico (Holycross et al. 2006, p. 3). Holycross et al.
(2006, p. 3) suspect the species was likely not historically present in
the lowest reaches of the Salt, Verde, and Gila rivers, even where
perennial flow persists. Numerous records for the narrow-headed
gartersnake (through 1996) in Arizona are maintained in the AGFD's
Heritage Database (1996b). The narrow-headed gartersnake as currently
recognized does not occur in Mexico.
Current Distribution and Population Status
Where narrow-headed gartersnakes are locally abundant, they can
usually be detected reliably and with significantly less effort than
populations characterized as having low densities. Narrow-headed
gartersnakes are well-camouflaged, secretive, and very difficult to
detect in structurally complex, dense habitat where they could occur at
very low population densities, which characterizes most occupied sites.
Water clarity can also affect survey accuracy. We considered factors
such as the date of the last known records for narrow-headed
gartersnakes in an area, as well as
[[Page 41508]]
records of one or more native prey species in making a conclusion on
species occupancy. We used all records that were dated 1980 or later
because the 1980s marked the first systematic survey efforts for
narrow-headed gartersnakes species across their range (see Rosen and
Schwalbe (1988, entire) and Fitzgerald (1986, entire)), and the last,
previous records were often dated several decades prior and may not
accurately represent the likelihood for current occupation. Several
areas where narrow-headed gartersnakes were known to occur have
received no, or very little, survey effort in the past several decades.
Variability in survey design and effort makes it difficult to compare
population sizes or trends among sites and between sampling periods.
Thus, for each of the sites discussed in Appendix A (available at
http://www.regulations.gov under Docket No. FWS-R2-ES-2013-0071), we
have attempted to translate and quantify search and capture efforts
into comparable units (i.e., person-search hours and trap-hours) and
have conservatively interpreted those results. Because the presence of
suitable prey species in an area may provide evidence that northern
Mexican gartersnake may still persist in low density where survey data
are sparse, a record of a native prey species was considered in our
determination of occupancy of this species.
Population status information, based on our review of the best
scientific and commercial data available, suggests that the narrow-
headed gartersnake has experienced significant declines in population
density and distribution along streams and rivers where it was formerly
well-documented and reliably detected. Many areas where the species may
occur likely rely on emigration of individuals from occupied habitat
into those areas to maintain the species, provided there are no
barriers to movement. Holycross et al. (2006) represents the most
recent, comprehensive survey effort for narrow-headed gartersnakes in
Arizona. Our most current information on the species' status in New
Mexico comes from a species expert who is completing a graduate degree
focused on the relationship between narrow-headed gartersnake
populations and fish communities in the upper Gila and San Francisco
river drainages (Helleckson 2012a, pers. comm.). Narrow-headed
gartersnakes were detected in only 5 of 16 historical localities in
Arizona and New Mexico surveyed by Holycross et al. (2006) in 2004 and
2005. Population densities have noticeably declined in many
populations, as compared to previous survey efforts (Holycross et al.
2006, p. 66). Holycross et al. (2006, pp. 66-67) compared narrow-headed
gartersnake detections based on results from their effort and that of
previous efforts in the same locations and found that significantly
more effort is required to detect this species in areas where it was
formerly robust, such as along Eagle Creek (AZ), the East Verde River
(AZ), the San Francisco River (NM), the Black River (AZ), and the Blue
River (AZ).
As of 2011, the only remaining narrow-headed gartersnake
populations where the species could reliably be found were located at:
(1) Whitewater Creek (New Mexico), (2) Tularosa River (New Mexico), (3)
Diamond Creek (New Mexico), (4) Middle Fork Gila River (New Mexico),
and (5) Oak Creek Canyon (Arizona). However, populations found in
Whitewater Creek and the Middle Fork Gila River were likely
significantly affected by New Mexico's largest wildfire in State
history, the Whitewater-Baldy Complex Fire, which occurred in June
2012. In addition, salvage efforts were initiated for these two
populations, which included the removal of 25 individuals from
Whitewater Creek and 14 individuals from the Middle Fork Gila River
before the onset of summer rains in 2012. The status of those
populations has likely deteriorated as a result of subsequent declines
in resident fish communities due to heavy ash and sediment flows,
resulting fish kills, and the removal of snakes, but subsequent survey
data have not been collected. If the Whitewater Creek and Middle Fork
Gila River populations did decline as a result of these factors, only
three remaining populations of this species remain viable today across
their entire distribution. Such unnaturally large wildfires have become
increasingly common across the Mogollon Rim of Arizona and New Mexico
where the narrow-headed gartersnake historically occurred. The status
of the narrow-headed gartersnake on tribal land is poorly known, due to
limited survey access.
In Table 2 below, we summarize the population status of the narrow-
headed gartersnake at all known localities throughout its distribution,
as supported by museum records or reliable observations. For a detailed
discussion that explains the rationale for site-by-site conclusions on
occupancy, please see Appendix A (available at http://www.regulations.gov under Docket No. FWS-R2-ES-2013-0071). General
rationale is provided in the introductory paragraph to this section,
``Current Distribution and Population Status.''
Table 2--Current Population Status of the Narrow-Headed Gartersnake. References Cited Are Provided in Appendix A
----------------------------------------------------------------------------------------------------------------
Suitable Harmful
Location Last record physical habitat Native prey nonnative Population
present species present species present status
----------------------------------------------------------------------------------------------------------------
West Fork Gila River (NM).... 2011 Yes............. Yes............ Yes............ Likely not
viable.
Middle Fork Gila River (NM).. 2012 Yes............. Yes............ Yes............ Likely not
viable.
East Fork Gila River (NM).... 2006 Yes............. Yes............ Yes............ Likely not
viable.
Gila River (AZ, NM).......... 2009 Yes............. Yes............ Yes............ Likely not
viable.
Snow Creek/Snow Lake (NM).... 2012 Yes............. No............. Yes............ Likely not
viable.
Gilita Creek (NM)............ 2009 Yes............. Yes............ No............. Likely not
viable.
Iron Creek (NM).............. 2009 Yes............. Yes............ No............. Likely not
viable.
Little Creek (NM)............ 2010 Yes............. Possible....... Yes............ Likely not
viable.
Turkey Creek (NM)............ 1985 Yes............. Yes............ Possible....... Likely not
viable.
Beaver Creek (NM)............ 1949 Yes............. Possible....... Yes............ Likely
extirpated.
Black Canyon (NM)............ 2010 Yes............. Yes............ No............. Likely not
viable.
Taylor Creek (NM)............ 1960 Yes............. No............. Yes............ Likely
extirpated.
Diamond Creek (NM)........... 2011 Yes............. Yes............ Yes............ Likely viable.
Tularosa River (NM).......... 2012 Yes............. Yes............ Yes............ Likely viable.
Whitewater Creek (NM)........ 2012 Yes............. Yes............ Yes............ Likely not
viable.
San Francisco River (NM)..... 2011 Yes............. Yes............ Yes............ Likely not
viable.
South Fork Negrito Creek (NM) 2011 Yes............. Possible....... Yes............ Likely not
viable.
[[Page 41509]]
Blue River (AZ).............. 2007 Yes............. Yes............ Yes............ Likely not
viable.
Dry Blue Creek (AZ, NM)...... 2010 Yes............. Possible....... Yes............ Likely not
viable.
Campbell Blue Creek (AZ, NM). 2010 Yes............. Possible....... Yes............ Likely not
viable.
Saliz Creek (NM)............. 2012 Yes............. Possible....... Yes............ Likely not
viable.
Eagle Creek (AZ)............. 1991 Yes............. Yes............ Yes............ Likely not
viable.
Black River (AZ)............. 2009 Yes............. Yes............ Yes............ Likely not
viable.
White River (AZ)............. 1986 Yes............. Yes............ Possible....... Likely not
viable.
Diamond Creek (AZ)........... 1986 Yes............. Possible....... Possible....... Likely not
viable.
Tonto Creek (tributary to Big 1915 Yes............. Possible....... Possible....... Likely
Bonita Creek, AZ). extirpated.
Canyon Creek (AZ)............ 1991 Yes............. Yes............ No............. Likely not
viable.
Upper Salt River (AZ)........ 1985 Yes............. Yes............ Yes............ Likely not
viable.
Cibeque Creek (AZ)........... 1991 Yes............. Yes............ Possible....... Likely not
viable.
Carrizo Creek (AZ)........... 1997 Yes............. Yes............ Possible....... Unreliably
detected.
Big Bonito Creek (AZ)........ 1957 Yes............. Yes............ Yes............ Likely
extirpated.
Haigler Creek (AZ)........... Early 1990s Yes............. Yes............ Yes............ Likely not
viable.
Houston Creek (AZ)........... 2005 Yes............. Yes............ Yes............ Likely not
viable.
Tonto Creek (tributary to 2005 Yes............. Yes............ Yes............ Likely not
Salt River, AZ). viable.
Deer Creek (AZ).............. 1995 No.............. No............. No............. Likely
extirpated.
Upper Verde River (AZ)....... 2012 Yes............. Yes............ Yes............ Likely not
viable.
Oak Creek (AZ)............... 2012 Yes............. Yes............ Yes............ Likely viable.
East Verde River (AZ)........ 1992 Yes............. Yes............ Yes............ Likely not
viable.
----------------------------------------------------------------------------------------------------------------
``Possible'' means there were no conclusive data found.
``Likely extirpated'' means the last record for an area pre-dated
1980 and existing threats suggest the species is likely extirpated.
``Likely not viable'' means there is a post-1980 record for the
species, it is not reliably found with minimal to moderate survey
effort, and threats exist which suggest the population may be low
density or could be extirpated, but there is insufficient evidence to
confirm extirpation. ``Likely viable'' means that the species is
reliably found with minimal to moderate survey effort and the
population is generally considered viable.
Table 2 lists the 38 known localities for narrow-headed
gartersnakes throughout their range. Appendix A (available at http://www.regulations.gov under Docket No. FWS-R2-ES-2013-0071) discusses
such considerations as the physical condition of habitat, the
composition of the aquatic biological community, the existence of
significant threats, and the length of time since the last known
observation of the species in presenting rationale for determining
occupancy status at each locality. We have concluded that in as many as
29 of 38 known localities (76 percent), the narrow-headed gartersnake
population is likely not viable and may exist at low population
densities that could be threatened with extirpation or may already be
extirpated but survey data are lacking in areas where access is
restricted. In most localities where the species may occur at low
population densities, existing survey data are insufficient to conclude
extirpation. As of 2012, narrow-headed gartersnake populations are
considered likely viable in 3 localities (8 percent) where individuals
are reliable detected. As displayed in Table 2, harmful nonnative
species are a concern for almost every narrow-headed gartersnake
population throughout their range. The ramifications of this are
significant because of the effect these harmful nonnative species have
on the resident native fish communities and the fact that this species
is a specialized, fish-only predator. We discuss this and other
important factors that have contributed to the decline of narrow-headed
gartersnakes throughout their range in our threats analysis below.
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.
In the following threats analysis, we treat both gartersnake
species in a combined discussion because of partially overlapping
ranges, similar natural histories, similar responses to threats, and
the fact that many threats are shared in common throughout their
ranges.
The Weakened Status of Native Aquatic Communities
Riparian and aquatic communities in both the United States and
Mexico have been significantly impacted by a shift in species'
composition, from one of primarily native fauna, to one being
increasingly dominated by an expanding assemblage of nonnative animal
species. Many of these nonnative species have been intentionally or
accidentally introduced, including crayfish, bullfrogs, and nonnative,
spiny-rayed fish. Harmful nonnative species have been introduced or
have spread into new areas through a variety of mechanisms, including
intentional and accidental releases, sport stocking, aquaculture,
aquarium releases, and bait-bucket release.
The occurrence of harmful nonnative species, such as the bullfrog,
the northern (virile) crayfish (Orconectes virilis), red swamp crayfish
(Procambarus clarkii), and numerous species of nonnative, spiny-rayed
fish,
[[Page 41510]]
has contributed to rangewide declines in both species of gartersnake,
and continues to be the most significant threat to the northern Mexican
and narrow-headed gartersnakes, and to their prey base, as a result of
direct predation, competition, and modification of habitat as evidenced
in a broad body of literature, the most recent of which extends from
1985 to the present (Meffe 1985, pp. 179-185; Propst et al. 1986, pp.
14-31, 82; 1988, p. 64; 2009, pp. 5-17; Minckley 1987, pp. 2, 16; 1993,
pp. 7-13; Rosen and Schwalbe 1988, pp. 28, 32; 1997, p. 1; Bestgen and
Propst 1989, pp. 409-410; Clarkson and Rorabaugh 1989, pp. 531, 535;
Papoulias et al. 1989, pp. 77-80; Marsh and Minckley 1990, p. 265;
Jakle 1992, pp. 3-5; 1995, pp. 5-7; ASU 1994, multiple reports; 1995,
multiple reports; 2008, multiple reports; Stefferud and Stefferud 1994,
p. 364; Douglas et al. 1994, pp. 9-19; Rosen et al. 1995, pp. 257-258;
1996b, pp. 2, 11-13; 2001, p. 2; Springer 1995, pp. 6-10; Degenhardt et
al. 1996, p. 319; Fernandez and Rosen 1996, pp. 8, 23-27, 71, 96;
Richter et al. 1997, pp. 1089, 1092; Weedman and Young 1997, pp. 1,
Appendices B, C; Inman et al. 1998, p. 17; Rinne et al. 1998, pp. 4-6;
2004, pp. 1-2; Jahrke and Clark 1999, pp. 2-7; Minckley et al. 2002,
pp. 696; Nowak and Santana-Bendix 2002, Table 3; Propst 2002, pp. 21-
25; DFT 2003, pp. 1-3, 5-6, 19; 2004, pp. 1-2, 4-5, 10, Table 1; 2006,
pp. iii, 25; Marsh et al. 2003, p. 667; Bonar et al. 2004, pp. 13, 16-
21; Rinne 2004, pp. 1-2; Clarkson et al. 2005, p. 20; 2008, pp. 3-4;
Fagan et al. 2005, pp. 34, 34-41; Knapp 2005, pp. 273-275; Olden and
Poff 2005, pp. 82-87; AGFD 2006, p. 83; Turner 2007, p. 41; Holycross
et al. 2006, pp. 13-15; Brennan and Holycross 2006, p. 123; Brennan
2007, pp. 5, 7; Turner and List 2007, p. 13; USFWS 2007, pp. 22-23;
Burger 2008, p. 4; Caldwell 2008a, 2008b; Duifhuis Rivera et al. 2008,
p. 479, Jones 2008b; d'Orgeix 2008; Haney et al. 2008, p. 59; Luja and
Rodr[iacute]guez-Estrella 2008, pp. 17-22; Probst et al. 2008, pp.
1242-1243; Rorabaugh 2008a, p. 25; USFS 2008; Wallace et al. 2008, pp.
243-244; Witte et al. 2008, p. 1; Bahm and Robinson 2009a, pp. 2-6;
2009b, pp. 1-4; Brennan and Rosen 2009, pp. 8-9; Karam et al. 2009; pp.
2-3; Minckley and Marsh 2009, pp. 50-51; Paroz et al. 2009, pp. 12, 18;
Robinson and Crowder 2009, pp. 3-5; Pilger et al. 2010, pp. 311-312;
Stefferud et al. 2011, pp. 11-12; C. Akins 2012, pers. comm.; Young and
Boyarski 2013, pp. 159-160; Emmons and Nowak 2013, p. 5).
The Decline of the Gartersnake Prey Base
The documented decline of the northern Mexican and narrow-headed
gartersnakes was typically subsequent to the declines in their prey
base (native amphibian and fish populations). These declines in prey
base result from predation following the establishment of nonnative
bullfrogs, crayfish, and numerous species of nonnative, spiny-rayed
fish as supported by an extensive body of literature referenced
immediately above.
Northern Mexican and narrow-headed gartersnakes appear to be
particularly vulnerable to the loss of native prey species (Rosen and
Schwalbe 1988, pp. 20, 44-45). Rosen et al. (2001, pp. 10, 13, 19)
examined this issue in detail with respect to the northern Mexican
gartersnake, and proposed two reasons for its decline following a loss
of, or decline in, the native prey base: (1) The species is unlikely to
increase foraging efforts at the risk of increased predation; and (2)
the species needs adequate food on a regular basis to maintain its
weight and health. If forced to forage more often for smaller prey
items, a reduction in growth and reproductive rates can result (Rosen
et al. 2001, pp. 10, 13). Rosen et al. (2001, p. 22) concluded that the
presence and expansion of nonnative predators (mainly bullfrogs,
crayfish, and green sunfish (Lepomis cyanellus)) is the primary cause
of decline in northern Mexican gartersnakes and their prey in
southeastern Arizona. In another example, Drummond and Marcias Garcia
(1983, pp. 25, 30) found that Mexican gartersnakes fed primarily on
frogs, and functioned as a local specialist in that regard. When frogs
became unavailable, the species simply ceased major foraging
activities. This led the author to conclude that frog abundance is
probably the most important correlate, and main determinant, of
foraging behavior in this species. Alternatively, terrestrial prey
species were consumed, but the gartersnakes were never documented as
having these prey items as a major dietary component, even when the
gartersnakes were in dire need (Drummond and Marcias Garcia 1983, p.
37).
With respect to narrow-headed gartersnakes, the relationship
between harmful nonnative species, a declining prey base, and
gartersnake populations is clearly depicted in one population along Oak
Creek. Nowak and Santana-Bendix (2002, Table 3) found a clear partition
in the distribution of nonnative, spiny-rayed fish and soft-rayed fish
in the vicinity of Midgely Bridge, where nonnative, spiny-rayed fish
increased in abundance in the downstream direction and soft-rayed fish
increased in abundance in the upstream direction. These fish community
distributions closely parallel that of narrow-headed gartersnakes along
Oak Creek, where gartersnake populations increase in density in the
upstream direction and decrease notably in the downstream direction
(Nowak and Santana-Bendix 2002, p. 23). Numerous historical records for
narrow-headed gartersnakes document the species in the lower reach of
Oak Creek, but the species is currently rarely detected in this reach
of Oak Creek (Nowak and Santana-Bendix 2002, pp. 13-14), providing
evidence of the decline of narrow-headed gartersnakes in the presence
of nonnative, spiny-rayed fish.
Fish--Northern Mexican and narrow-headed gartersnakes can
successfully use nonnative, soft-rayed fish species as prey, including
mosquitofish, red shiner, and introduced trout (Salmo sp.) (Nowak and
Santana-Bendix 2002, pp. 24-25; Holycross et al. 2006, p. 23). However,
all other nonnative species, most notably the spiny-rayed fish, are not
considered prey species for northern Mexican or narrow-headed
gartersnakes and, in addition, are known to prey on neonatal and
juvenile gartersnakes. Nowak and Santana-Bendix (2002, p. 24) propose
two hypotheses regarding the reluctance of narrow-headed gartersnakes
to prey on nonnative, spiny-rayed fish: (1) The laterally-compressed
shape and presence of sharp, spiny dorsal spines present a choking
hazard to gartersnakes that has been observed to be fatal; and (2)
nonnative, spiny-rayed fish tend to occupy the middle and upper zones
in the water column, while narrow-headed gartersnakes typically hunt
along the bottom (where native fish tend to occur). As a result,
nonnative, spiny-rayed fish may be largely ecologically unavailable as
prey. It is likely the shape and presence of sharp, spiny dorsal spines
on these nonnative fish species also present a choking hazard to both
northern Mexican and narrow-headed gartersnakes.
Nonnative, spiny-rayed fish invasions can indirectly affect the
health, maintenance, and reproduction of northern Mexican and narrow-
headed gartersnakes by altering their foraging strategy and
compromising foraging success. Rosen et al. (2001, p. 19), in
addressing the northern Mexican gartersnake, proposed that an increase
in energy expended in foraging, coupled by the reduced number of small
to
[[Page 41511]]
medium-sized prey fish available, results in deficiencies in nutrition,
affecting growth and reproduction. This occurs because energy is
allocated to maintenance and the increased energy costs of intense
foraging activity, rather than to growth and reproduction. In contrast,
a northern Mexican gartersnake diet that includes both fish and
amphibians, such as leopard frogs, reduces the necessity to forage at a
higher frequency, allowing metabolic energy gained from larger prey
items to be allocated instead to growth and reproductive development.
Myer and Kowell (1973, p. 225) experimented with food deprivation in
common gartersnakes, and found significant reductions in lengths and
weights of juvenile snakes that were deprived of regular feedings
versus the control group that were fed regularly at natural
frequencies. Reduced foraging success of both northern Mexican and
narrow-headed gartersnakes means that individuals are likely to become
vulnerable to effects from starvation, which may increase mortality
rates of juveniles and, consequently, affect recruitment.
Northern Mexican gartersnakes have a more varied diet than narrow-
headed gartersnakes. We are not aware of any studies that have
addressed the direct relationship between prey base diversity and
northern Mexican gartersnake recruitment and survivorship. However,
Krause and Burghardt (2001, pp. 100-123) discuss the benefits and costs
that may be associated with diet variability in the common gartersnake
(Thamnophis sirtalis), an ecologically similar species to the northern
Mexican gartersnake. Foraging for mixed-prey species may impede
predator learning, as compared to specialization, on a certain prey
species, but may also provide long-term benefits (Krause and Burghardt
2001, p. 101). Krause and Burghardt (2001, p. 112) stated that varied
predatory experience played an important role in the feeding abilities
of gartersnakes through the first 8 months of age. These data suggest
that a varied prey base might also be important for neonatal and
juvenile northern Mexican gartersnakes (also a species with a varied
diet) and that decreases in the diversity of the prey base during the
young age classes might adversely affect the ability of individuals to
capture prey throughout their lifespan, in addition to the more obvious
effects of reduced prey availability.
A wide variety of native fish species, now listed as endangered,
threatened, or candidates for listing, were historically primary prey
species for northern Mexican and narrow-headed gartersnakes (Rosen and
Schwalbe 1988, pp. 18, 39). Aquatic habitat destruction and
modification is often considered a leading cause for the decline in
native fish in the southwestern United States. However, Marsh and Pacey
(2005, p. 60) predict that despite the significant physical alteration
of aquatic habitat in the southwest, native fish species could not only
complete all of their life functions but could flourish in these
altered environments, but for the presence of (harmful) nonnative fish
species, as supported by a ``substantial and growing body of evidence
derived from case studies.'' Northern Mexican and narrow-headed
gartersnakes depend on native fish as a principle part of their prey
base, although nonnative, soft-rayed fish are also common prey items
where they overlap in distribution with these gartersnakes (Nowak and
Santana-Bendix 2002, pp. 24-25; Holycross et al. 2006, p. 23).
Nonnative, spiny-rayed fish compete with northern Mexican and narrow-
headed gartersnakes for prey. In their extensive surveys, Rosen and
Schwalbe (1988, p. 44) only found narrow-headed gartersnakes in
abundance where native fish species predominated, but did not find them
abundant in the presence of robust nonnative, spiny-rayed fish
populations. Minckley and Marsh (2009, pp. 50-51) found nonnative
fishes to be the single-most significant factor in the decline of
native fish species and also their primary obstacle to recovery. Of the
48 conterminous States in the United States, Arizona has the highest
proportion of nonnative fish species (66 percent) represented by
approximately 68 species of nonnative fish (Turner and List 2007, p.
13).
Collier et al. (1996, p. 16) note that interactions between native
and nonnative fish have significantly contributed to the decline of
many native fish species from direct predation and, indirectly, from
competition (which has adversely affected the prey base for northern
Mexican and narrow-headed gartersnakes). The AGFD considers native fish
in Arizona as the most threatened taxa among the State's native
species, largely as a result of predation and competition with
nonnative species (AGFD 2006, p. 83). Holycross et al. (2006, pp. 52-
61) documented significantly depressed or extirpated native fish prey
bases for northern Mexican and narrow-headed gartersnakes along the
Mogollon Rim in Arizona and New Mexico. Rosen et al. (2001, Appendix I)
documented the decline of several native fish species in several
locations visited in southeastern Arizona, further affecting the prey
base of northern Mexican gartersnakes in that area.
Stocked for sport, forage, or biological control, nonnative fishes
have been shown to become invasive where released, do not require
natural flow regimes, and tend to be more phylogenetically advanced
than native species (Kolar et al. 2003, p. 9) which contributed to
their expansion in the Gila River basin. Harmful nonnative fish species
tend to be nest-builders and actively guard their young which may
provide them another ecological advantage over native species which are
broadcast spawners and provide no parental care to their offspring
(Marsh and Pacey 2005, p. 60). It is therefore likely that recruitment
and survivorship is greater in nonnative species than native species
where they overlap, providing them with an ecological advantage. Table
2-1 in Kolar et al. (2003, p. 10) provides a map depicting the high
degree of overlap in the distribution of native and nonnative fishes
within the Gila River basin of Arizona and New Mexico as well as
watersheds thought to be dominated by nonnative fish species. The
widespread decline of native fish species from the arid southwestern
United States and Mexico has resulted largely from interactions with
nonnative species and has been captured in the listing rules of 13
native species listed under the Act, and whose historical ranges
overlap with the historical distribution of northern Mexican and
narrow-headed gartersnakes. Native fish species that were likely prey
species for these gartersnakes and are now listed under the Act,
include the bonytail chub (Gila elegans, 45 FR 27710, April 23, 1980),
Yaqui catfish (Ictalurus pricei, 49 FR 34490, August 31, 1984), Yaqui
chub (Gila purpurea, 49 FR 34490, August 31, 1984), Yaqui topminnow
(Poeciliopsis occidentalis sonoriensis, 32 FR 4001, March 11, 1967),
beautiful shiner (Cyprinella formosa, 49 FR 34490, August 31, 1984),
humpback chub (Gila cypha, 32 FR 4001, March 11, 1967), Gila chub (Gila
intermedia, 70 FR 66663, November 2, 2005), Colorado pikeminnow
(Ptychocheilus lucius, 32 FR 4001, March 11, 1967), spikedace (Meda
fulgida, 77 FR 10810, February 23, 2012), loach minnow (Tiaroga
cobitis, 77 FR 10810, February 23, 2012), razorback sucker (Xyrauchen
texanus, 56 FR 54957, October 23, 1991), desert pupfish (Cyprinodon
macularius, 51 FR 10842, March 31, 1986), and Gila topminnow
(Poeciliopsis occidentalis, 32 FR 4001, March 11, 1967). In total,
within Arizona, 19 of 31 (61 percent) native
[[Page 41512]]
fish species are listed under the Act. Arizona ranks the highest of all
50 States in the percentage of native fish species with declining
trends (85.7 percent) and New Mexico ranks sixth (48.1 percent) (Stein
2002, p. 21; Warren and Burr 1994, p. 14). Recovery of native fishes in
the Southwest has been fraught with complicating factors, both natural
and sociopolitical, which have presented significant challenges to the
recovery of many imperiled native fish species (Minckley and Marsh
2009, pp. 52-53), including many that are important prey species for
the northern Mexican and narrow-headed gartersnakes.
In an evolutionary context, many native fishes co-evolved with very
few predatory fish species, whereas most of the nonnative species co-
evolved with many predatory species (Clarkson et al. 2005, p. 21). A
contributing factor to the decline of native fish species cited by
Clarkson et al. (2005, p. 21) is that most of the nonnative species
evolved behaviors, such as nest guarding, to protect their offspring
from these many predators, while native species are generally broadcast
spawners that provide no parental care. In the presence of nonnative
species, the reproductive behaviors of native fish fail to allow them
to compete effectively with the nonnative species, and, as a result,
the viability of native fish populations is reduced.
Olden and Poff (2005, p. 75) stated that environmental degradation
and the proliferation of nonnative fish species threaten the highly
localized and unique fish faunas of the American Southwest. The fastest
expanding nonnative species are red shiner (Cyprinella lutrensis),
fathead minnow (Pimephales promelas), green sunfish, largemouth bass
(Micropterus salmoides), western mosquitofish, and channel catfish
(Ictalurus punctatus). These species are considered to be the most
invasive in terms of their negative impacts on native fish communities
(Olden and Poff 2005, p. 75). Many nonnative fishes, in addition to
those listed immediately above, including yellow and black bullheads
(Ameiurus sp.), flathead catfish (Pylodictis olivaris), and smallmouth
bass (Micropterus dolomieu), have been introduced into formerly and
currently occupied northern Mexican or narrow-headed gartersnake
habitat and are predators on these species and their prey (Bestgen and
Propst 1989, pp. 409-410; Marsh and Minckley 1990, p. 265; Sublette et
al. 1990, pp. 112, 243, 246, 304, 313, 318; Abarca and Weedman 1993,
pp. 6-12; Stefferud and Stefferud 1994, p. 364; Weedman and Young 1997,
pp. 1, Appendices B, C; Rinne et al. 1998, pp. 3-6; Voeltz 2002, p. 88;
Bonar et al. 2004, pp. 1-108; Fagan et al. 2005, pp. 34, 38-39, 41;
Probst et al. 2008, pp. 1242-1243). Nonnative, spiny-rayed fish
species, such as flathead catfish, may be especially dangerous to
narrow-headed gartersnake populations through competition and direct
predation, because they are primarily piscivorous (fish-eating) (Pilger
et al. 2010, pp. 311-312), have large mouths, and have a tendency to
occur along the stream bottom, where narrow-headed gartersnakes
principally forage.
Rosen et al. (2001, Appendix I) and Holycross et al. (2006, pp. 15-
51) conducted large-scale surveys for northern Mexican gartersnakes in
southeastern and central Arizona and narrow-headed gartersnakes in
central and east-central Arizona, and documented the presence of
nonnative fish at many locations. Holycross et al. (2006, pp. 14-15)
found nonnative fish species in 64 percent of the sample sites in the
Agua Fria subbasin, 85 percent of the sample sites in the Verde River
subbasin, 75 percent of the sample sites in the Salt River subbasin,
and 56 percent of the sample sites in the Gila River subbasin. In
total, nonnative fish were observed at 41 of the 57 sites surveyed (72
percent) across the Mogollon Rim (Holycross et al. 2006, p. 14).
Entirely native fish communities were detected in only 8 of 57 sites
surveyed (14 percent) (Holycross et al. 2006, p. 14). It is well
documented that nonnative fish have now infiltrated the majority of
aquatic communities in the southwestern United States as depicted in
Tables 1 and 2, above, as well as in Appendix A (available at http://www.regulations.gov under Docket No. FWS-R2-ES-2013-0071).
Several authors have identified both the presence of nonnative fish
as well as their deleterious effects on native species within Arizona.
Many areas have seen a shift from a predominance of native fishes to a
predominance of nonnative fishes. On the upper Verde River, native
species dominated the total fish community at greater than 80 percent
from 1994 to 1996, before dropping to approximately 20 percent in 1997
and 19 percent in 2001. At the same time, three nonnative species
increased in abundance between 1994 and 2000 (Rinne et al. 2004, pp. 1-
2). In an assessment of the Verde River, Bonar et al. (2004, p. 57)
found that in the Verde River mainstem, nonnative fishes were
approximately 2.6 times more dense per unit volume of river than native
fishes, and their populations were approximately 2.8 times that of
native fishes per unit volume of river. Haney et al. (2008, p. 61)
declared the northern Mexican gartersnake as nearly lost from the Verde
River but also suggested that diminished river flow may be an important
factor. Similar changes in the dominance of nonnative fishes have
occurred on the Middle Fork Gila River, with a 65 percent decline of
native fishes between 1988 and 2001 (Propst 2002, pp. 21-25). Abarca
and Weedman (1993, pp. 6-12) found that the number of nonnative fish
species was twice the number of native fish species in Tonto Creek in
the early 1990s, with a stronger nonnative species influence in the
lower reaches, where the northern Mexican gartersnake is considered to
still occur, and Burger (2008, p. 8) confirmed their continued
existence there. Surveys in the Salt River above Lake Roosevelt
indicate a decline of roundtail chub and other natives with an increase
in flathead and channel catfish numbers (Voeltz 2002, p. 49).
In New Mexico, nonnative fish have been identified as the main
cause for declines observed in native fish populations (Voeltz 2002, p.
40; Probst et al. 2008, pp. 1242-1243). Fish experts from the U.S.
Forest Service, U.S. Bureau of Reclamation, U.S. Bureau of Land
Management (BLM), University of Arizona, Arizona State University, the
Nature Conservancy, and others declared the native fish fauna of the
Gila River basin to be critically imperiled, and they cite habitat
destruction and nonnative species as the primary factors for the
declines. They call for the control and removal of nonnative fish as an
overriding need to prevent the decline, and ultimate extinction, of
native fish species within the basin (DFT 2003, p. 1). In some areas,
nonnative fishes may not dominate the system, but their abundance has
increased. This is the case for the Cliff-Gila Valley area of the Gila
River, where nonnative fishes increased from 1.1 percent to 8.5
percent, while native fishes declined steadily over a 40-year period
(Propst et al. 1986, pp. 27-32). At the Redrock and Virden valleys on
the Gila River, the relative abundance in nonnative fishes in the same
time period increased from 2.4 percent to 17.9 percent (Propst et al.
1986, pp. 32-34). Four years later, the relative abundance of nonnative
fishes increased to 54.7 percent at these sites (Propst et al. 1986,
pp. 32-36). The percentage of nonnative fishes increased by almost 12
percent on the Tularosa River between 1988 and 2003, while on the East
Fork Gila River, nonnative fishes increased to 80.5 percent relative
abundance in 2003 (Propst 2005, pp. 6-7, 23-24).
[[Page 41513]]
Nonnative fishes are also considered a management issue in other areas
including Eagle Creek, the San Pedro River, West Fork Gila River, and
to a lesser extent, the Blue River.
In addition to harmful nonnative species, various parasites may
affect native fish species that are prey for northern Mexican and
narrow-headed gartersnakes. Asian tapeworm was introduced into the
United States with imported grass carp (Ctenopharyngodon idella) in the
early 1970s. It has since become well established in areas throughout
the southwestern United States. The definitive host in the life cycle
of Asian tapeworm is a cyprinid fish (carp or minnow), and therefore it
is a potential threat to native cyprinids in Arizona and New Mexico.
The Asian tapeworm adversely affects fish health by impeding the
digestion of food as it passes through the digestive track. Emaciation
and starvation of the host can occur when large enough numbers of worms
feed off the fish directly. An indirect effect is that weakened fish
are more susceptible to infection by other pathogens. Asian tapeworm
invaded the Gila River basin and was found during the Central Arizona
Project's fall 1998 monitoring in the Gila River at Ashurst-Hayden Dam.
It has also been confirmed from Bonita Creek in 2010 (USFWS National
Wild Fish Health Survey 2010). This parasite can infect many species of
fish and is carried into new areas along with nonnative fishes or
native fishes from contaminated areas.
Another parasite (Ichthyophthirius multifiliis) (Ich) usually
occurs in deep waters with low flow and is a potential threat to native
fish. Ich has occurred in some Arizona streams, probably encouraged by
high temperatures and crowding as a result of drought. This parasite
was observed being transmitted on the Sonora sucker (Catostomus
insignis), although it does not appear to be host-specific and could be
transmitted by other species (Mpoame 1982, p. 46). It has been found on
desert and Sonoran suckers, as well as roundtail chub (Robinson et al.
1998, p. 603), which are important prey species for the northern
Mexican and narrow-headed gartersnakes. This parasite becomes embedded
under the skin and within the gill tissues of infected fish. When Ich
matures, it leaves the fish, causing fluid loss, physiological stress,
and sites that are susceptible to infection by other pathogens. If Ich
is present in large enough numbers, it can also impact respiration
because of damaged gill tissue.
Anchor worm (Lernaea cyprinacea), an external parasite, is unusual
in that it has little host specificity, infecting a wide range of
fishes and amphibians. Infection by this parasite has been known to
kill large numbers of fish due to tissue damage and secondary infection
of the attachment site (Hoffnagle and Cole 1999, p. 24). Presence of
this parasite in the Gila River basin is a threat to native fishes. In
July 1992, the BLM found anchor worms in Bonita Creek. They have also
been documented in the Verde River (Robinson et al. 1998, pp. 599, 603-
605).
The yellow grub (Clinostomum marginatum) is a parasitic, larval
flatworm that appears as yellow spots on the body and fins of a fish.
Because the intermediate host is a bird and therefore highly mobile,
yellow grubs are easily spread. When yellow grubs infect a fish, they
penetrate the skin and migrate into its tissues, causing damage and
potentially hemorrhaging. Damage from one yellow grub may be minimal,
but in greater numbers, yellow grubs can kill fish (Maine Department of
Inland Fisheries and Wildlife 2002a, p. 1). Yellow grubs occur in many
areas in Arizona and New Mexico, including Oak Creek (Mpoame and Rinne
1983, pp. 400-401), the Salt River (Amin 1969, p. 436; Bryan and
Robinson 2000, p. 19), the Verde River (Bryan and Robinson 2000, p.
19), and Bonita Creek (Robinson 2011, pers. comm.).
The black grub (Neascus spp.), also called black spot, is a
parasitic larval fluke that appears as black spots on the skin, tail
base, fins, and musculature of a fish. When an intermediate life stage
of black grubs migrates into the tissues of a fish they are called
``cercaria.'' The damage caused by one cercaria is negligible, but in
greater numbers they may kill a fish (Lane and Morris 2000, pp. 2-3;
Maine Department of Inland Fisheries and Wildlife 2002b, p. 1). Black
grubs are present in the Verde River (Robinson et al. 1998, p. 603;
Bryan and Robinson 2000, p. 21), and are prevalent in the San Francisco
River in New Mexico (Paroz 2011, pers. comm.).
To date, we have no information on the effect of parasite
infestation in native fish on both gartersnake populations.
The Decline of Native Fish Communities in Mexico--The first
tabulations of freshwater fish species at risk in Mexico occurred in
1961, when 11 species were identified as being at risk (Contreras-
Balderas et al. 2003, p. 241). As of 2003, of the 506 species of
freshwater fish recorded in Mexico, 185 (37 percent) have been listed
by the Mexican Federal Government as either endangered, facing
extinction, under special protection, or likely extinct (Alvarez-Torres
et al. 2003, p. 323), almost a 17-fold increase in slightly over four
decades; 25 species are believed to have gone extinct (Contreras-
Balderas et al. 2003, p. 241). In the lower elevations of Mexico,
within the distribution of the northern Mexican gartersnake, there are
approximately 200 species of native freshwater fish documented, with
120 native species under some form of threat and an additional 15 that
have gone extinct (Contreras-Balderas and Lozano 1994, pp. 383-384).
The Fisheries Law in Mexico empowered the country's National Fisheries
Institute to compile and publish the National Fisheries Chart in 2000,
which found that Mexico's fish fauna has seriously deteriorated as a
result of environmental impacts (pollution), water basin degradation
(dewatering, siltation), and the introduction of nonnative species
(Alvarez-Torres et al. 2003, pp. 320, 323). The National Fisheries
Chart is regarded as the first time the Mexican government has openly
revealed the status of its freshwater fisheries and described their
management policies (Alvarez-Torres et al. 2003, pp. 323-324).
Industrial, municipal, and agricultural water pollution, dewatering
of aquatic habitat, and the proliferation nonnative species are widely
considered to be the greatest threats to freshwater ecosystems in
Mexico (Branson et al. 1960, p. 218; Conant 1974, pp. 471, 487-489;
Miller et al. 1989, pp. 25-26, 28-33; 2005, pp. 60-61; DeGregorio 1992,
p. 60; Contreras Balderas and Lozano 1994, pp. 379-381; Lyons et al.
1995, p. 572; 1998, pp. 10-12; va Landa et al. 1997, p. 316; Mercado-
Silva et al. 2002, p. 180; Contreras-Balderas et al. 2003, p. 241;
Dom[iacute]nguez-Dom[iacute]nguez et al. 2007, Table 3). A shift in
land use policies in Mexico to encourage free market principles in
rural, small-scale agriculture has been found to promote land use
practices that threaten local biodiversity (Ortega-Huerta and Kral
2007, p. 2; Randall 1996, pp. 218-220; Kiernan 2000, pp. 13-23). These
threats have been documented throughout the distribution of the
northern Mexican gartersnake in Mexico and are best represented in the
scientific literature in the context of fisheries studies. Contreras-
Balderas et al. (2003, pp. 241, 243) named Chihuahua (46 species),
Coahuila (35 species), Sonora (19 species), and Durango (18 species) as
Mexican states that had some of the most reports of freshwater fish
species at risk. These states are all within the distribution of the
northern Mexican gartersnake, indicating an overlapping trend of
declining prey bases and
[[Page 41514]]
threatened ecosystems within the range of the northern Mexican
gartersnake in Mexico. Contreras-Balderas et al. (2003, Appendix 1)
found various threats to be adversely affecting the status of
freshwater fish and their habitat in several states in Mexico: (1)
Habitat reduction or alteration (Sonora, Chihuahua, Durango, Coahuila,
San Luis Potos[iacute], Jalisco, Guanajuato); (2) water depletion
(Chihuahua, Durango, Coahuila, Sonora, Guanajuato, Jalisco, San Luis
Potos[iacute]); (3) harmful nonnative species (Durango, Chihuahua,
Coahuila, San Luis Potos[iacute], Sonora, Veracruz); and (4) pollution
(M[eacute]xico, Jalisco, Chihuahua, Coahuila, Durango). Within the
states of Chihuahua, Durango, Coahuila, Sonora, Jalisco, and
Guanajuato, water depletion is considered serious, with entire basins
having been dewatered, or conditions have been characterized as
``highly altered'' (Contreras-Balderas et al. 2003, Appendix 1). All of
the Mexican states with the highest numbers of fish species at risk are
considered arid, a condition hastened by increasing desertification
(Contreras-Balderas et al. 2003, p. 244).
Aquaculture and Nonnative Fish Proliferation in Mexico--Nonnative
fish compete with and prey upon northern Mexican gartersnakes and their
native prey species. The proliferation of nonnative fish species
throughout Mexico happened mainly by natural dispersal, intentional
stockings, and accidental breaches of artificial or constructed
barriers by nonnative fish. Lentic water bodies such as lakes,
reservoirs, and ponds are often used for flood control, agricultural
purposes, and most commonly to support commercial fisheries. The most
recent estimates indicate that Mexico has 13,936 of such water bodies,
where approximately 96 percent are between 2.47-247 acres (1-100
hectares) and approximately half are artificial (Sugunan 1997, Table
8.3; Alvarez-Torres et al. 2003, pp. 318, 322). Areas where these
landscape features are most prevalent occur within the distribution of
the northern Mexican gartersnake. For example, Jalisco and Zacatecas
are listed as two of four states with the highest number of reservoirs,
and Chihuahua is one of two states known for a high concentration of
lakes (Sugunan 1997, Section 8.4.2). Based on the data presented in
Sugunan (1997, Table 8.5), a total of 422 dammed reservoirs are located
within the 16 Mexican states where the northern Mexican gartersnake is
thought to occur. Mercado-Silva et al. (2006, p. 534) found that within
the state of Guanajuato, ``Practically all streams and rivers in the
[Laja] basin are truncated by reservoirs or other water extraction and
storage structures.'' On the Laja River alone, there are two major
reservoirs and a water diversion dam; 12 more reservoirs are located on
its tributaries (Mercado-Silva et al. 2006, p. 534). As a consequence
of dam operations, the main channel of the Laja remains dry for
extensive periods of time (Mercado-Silva et al. 2006, p. 541). The
damming and modification of the lower Colorado River in Mexico, where
the northern Mexican gartersnake occurred, has facilitated the
replacement of the entire native fishery with nonnative species (Miller
et al. 2005, p. 61). Each reservoir created by a dam is either managed
as a nonnative commercial fishery or has become a likely source
population of nonnative species, which have naturally or artificially
colonized the reservoir, dispersed into connected riverine systems, and
damaged native aquatic communities.
Mexico, as with other developing countries, depends in large part
on freshwater commercial fisheries as a source of protein for both
urbanized and rural human populated areas. Commercial and subsistence
fisheries rely heavily on introduced, nonnative species in the largest
freshwater lakes (Soto-Galera et al. 1999, p. 133) down to rural, small
ponds (Tapia and Zambrano 2003, p. 252). At least 87 percent of the
species captured or cultivated in inland fisheries of Mexico from 1989-
1999 included tilapia, common carp, channel catfish, trout, and black
bass (Micropterus sp.), all of which are nonnative (Alvarez-Torres et
al. 2003, pp. 318, 322). In fact, the northern and central plateau
region of Mexico (which comprises most of the distribution of the
northern Mexican gartersnake's distribution in Mexico) is considered
ideal for the production of harmful, predatory species such as bass and
catfish (Sugunan 1997, Section 8.3). Largemouth bass are now produced
and stocked in reservoirs and lakes throughout the distribution of the
northern Mexican gartersnake (Sugunan 1997, Section 8.8.1). The
Secretariat for Environment, Natural Resources and Fisheries, formed in
1995 and known as SEMARNAP, is the Mexican federal agency responsible
for management of the country's environment and natural resources.
SEMARNAP dictates the stocking rates of nonnative species into the
country's lakes and reservoirs. For example, the permitted stocking
rate for largemouth bass in Mexico is one fish per square meter in
large reservoirs (Sugunan 1997, Table 8.8); therefore, a 247-acre (100-
ha) reservoir could be stocked with 1,000,000 largemouth bass. The
common carp, the subject of significant aquaculture investment since
the 1960s in Mexico, is known for altering aquatic habitat and
consuming the eggs and fry of native fish species, and is now
established in 95 percent of Mexico's freshwater systems (Tapia and
Zambrano 2003, p. 252).
Basins in northern Mexico, such as the Rio Yaqui, have been found
to be significantly compromised by harmful nonnative fish species.
Unmack and Fagan (2004, p. 233) compared historical museum collections
of nonnative fish species from the Gila River basin in Arizona and the
Yaqui River basin in Sonora, Mexico, to gain insight into the trends in
distribution, diversity, and abundance of nonnative fishes in each
basin over time. They found that nonnative species are slowly, but
steadily, increasing in all three parameters in the Yaqui Basin (Unmack
and Fagan 2004, p. 233). Unmack and Fagan (2004, p. 233) predicted
that, in the absence of aggressive management intervention, significant
extirpations or range reductions of native fish species are expected to
occur in the Yaqui Basin of Sonora, Mexico, which may have extant
populations of the northern Mexican gartersnake, as did much of the
Gila Basin before the introduction of nonnative species. Loss of native
fishes will impact prey availability for the northern Mexican
gartersnake and threaten its persistence in these areas. Black
bullheads (Ameiurus melas) were reported as abundant, and common carp
were detected from the Rio Yaqui in southern Sonora, Mexico (Branson et
al. 1960, p. 219). Bluegill (Lepomis macrochirus) were also reported at
this location, representing a significant range expansion that the
authors expected was the result of escaping nearby farm ponds or
irrigation ditches (Branson et al. 1960, p. 220). Largemouth bass,
green sunfish, and an undetermined crappie species have also been
reported from this area (Branson et al. 1960, p. 220). Hendrickson and
Varela-Romero (1989, p. 479) conducted fish sampling along the
R[iacute]o Sonoyta of northern Sonora, Mexico, and found over half of
the fish collected were nonnative, both predatory species and prey
species for the northern Mexican gartersnake.
Dom[iacute]nguez-Dom[iacute]nguez et al. (2007, p. 171) sampled 52
localities for a rare freshwater fish, the Picotee goodeid
(Zoogoneticus quitzeoensis), along the southern portion of the Mesa
Central (Mexican Plateau) of Mexico and found 21 localities had
significant signs of pollution. Of the 29 localities where the target
species was detected, 28 of them also had harmful nonnative species
[[Page 41515]]
present, such as largemouth bass, cichlids (Oreochromis sp.), bluegill,
P[aacute]tzcuaro chub (Algansea lacustris) (Dom[iacute]nguez-
Dom[iacute]nguez et al. 2007, pp. 171, Table 3). Other nonnative fish
species reported are soft-rayed and small bodied, and may be prey items
for younger age classes of northern Mexican gartersnakes. Several
examples of significant aquatic habitat degradation or destruction were
also observed by Dom[iacute]nguez-Dom[iacute]nguez et al. (2007, Table
3) in this region of Mexico, including the draining of natural lakes
and cienegas for conversion to agricultural purposes, modification of
springs for recreational swimming, diversions, and dam construction. As
of 2006, native fish species comprised the most prevalent in species
composition and abundance in the Laja Basin; however the basin is
trending towards a nonnative fishery based on historical data whereas
nonnative species were most recently collected from 16 of 17 sample
sites, largemouth bass have significantly expanded their distribution
within the headwaters of the basin, and bluegill are now widespread in
the Laja River (Mercado-Silva et al. 2006, pp. 537, 542, Table 4).
The ecological risk of nonnative, freshwater aquaculture production
has only recently been acknowledged by the Mexican government as
compared to decades of aquaculture production, mainly because
conservation of biodiversity was not valued as highly as the benefits
garnered by nonnative fish production, most notably in the country's
rural, poorest regions (Tapia and Zambrano 2003, p. 252). In fact,
recent amendments to Mexico's fishing regulations allow for relaxation
of existing regulations imposed by other government regulations and
expansion of opportunities for investment in commercial fishing to
promote growth in Mexico's aquaculture sector (Sugunan 1997, Section
8.7.1). Between the broad geographic extent of commercial or sustenance
fisheries, the important source of protein they represent, and the many
mechanisms introduced nonnative fish have to naturally or artificially
expand their distribution, few areas within the range of the northern
Mexican gartersnake in Mexico have avoided adverse impacts associated
with nonnative species. Harmful nonnative fish species therefore pose a
significant threat to the prey base of northern Mexican gartersnakes
and to the gartersnakes themselves throughout most of their range in
Mexico.
Amphibian decline--Matthews et al. (2002, p. 16) examined the
relationship of gartersnake distributions, amphibian population
declines, and nonnative fish introductions in high-elevation aquatic
ecosystems in California. Matthews et al. (2002, p. 16) specifically
examined the effect of nonnative trout introductions on populations of
amphibians and mountain gartersnakes (Thamnophis elegans elegans).
Their results indicated the probability of observing gartersnakes was
30 times greater in lakes containing amphibians than in lakes where
amphibians have been extirpated by nonnative fish. These results
supported a prediction by Jennings et al. (1992, p. 503) that native
amphibian declines will lead directly to gartersnake declines. Matthews
et al. (2002, p. 20) noted that, in addition to nonnative fish species
adversely impacting amphibian populations that are part of the
gartersnake's prey base, direct predation on gartersnakes by nonnative
fish also occurs. However, Shah et al. (2010, pp. 188-190) found that
native tadpoles may exhibit anti-predator learning behavior that may
assist their persistence in habitat affected by nonnative, spiny-rayed
fish.
Declines in the native leopard frog populations in Arizona have
contributed to declines in the northern Mexican gartersnake, one of the
frog's primary native predators. Native ranid frog species, such as
lowland leopard frogs, northern leopard frogs, and federally threatened
Chiricahua leopard frogs, have all experienced declines in various
degrees throughout their distribution in the Southwest, partially due
to predation and competition with nonnative species (Clarkson and
Rorabaugh 1989, pp. 531, 535; Hayes and Jennings 1986, p. 490). Rosen
et al. (1995, pp. 257-258) found that Chiricahua leopard frog
distribution in the Chiricahua Mountain region of Arizona was inversely
related to nonnative species distribution and, without corrective
action, predicted that the Chiricahua leopard frog may be difficult to
conserve in this region. Along the Mogollon Rim, Holycross et al.
(2006, p. 13) found that only 8 sites of 57 surveyed (15 percent)
consisted of an entirely native anuran community, and that native frog
populations in another 19 sites (33 percent) had been completely
displaced by invading bullfrogs. However, such declines in native frog
populations are not necessarily irreversible. Ranid frog populations
have been shown to rebound strongly when nonnative fish are removed
(Knapp et al. 2007, pp. 15-18).
Scotia Canyon, in the Huachuca Mountains of southeastern Arizona,
is a location where corresponding declines of leopard frog and northern
Mexican gartersnake populations have been documented through repeated
survey efforts over time (Holm and Lowe 1995, p. 33). Surveys of Scotia
Canyon occurred during the early 1980s, and again during the early
1990s. Leopard frogs in Scotia Canyon were infrequently observed during
the early 1980s, and were apparently extirpated by the early 1990s
(Holm and Lowe 1995, pp. 45-46). Northern Mexican gartersnakes were
observed in decline during the early 1980s, with low capture rates
continuing through the early 1990s (Holm and Lowe 1995, pp. 27-35).
Surveys documented further decline of leopard frogs and northern
Mexican gartersnakes in 2000 (Rosen et al. 2001, pp. 15-16).
A former large, local population of northern Mexican gartersnakes
at the San Bernardino National Wildlife Refuge (SBNWR) in southeastern
Arizona has also experienced a correlative decline of leopard frogs,
and northern Mexican gartersnakes are now thought to occur at very low-
population densities or may be extirpated there (Rosen and Schwalbe
1988, p. 28; 1995, p. 452; 1996, pp. 1-3; 1997, p. 1; 2002b, pp. 223-
227; 2002c, pp. 31, 70; Rosen et al. 1996b, pp. 8-9; 2001, pp. 6-10).
Survey data indicate that declines of leopard frog populations,
often correlated with nonnative species introductions, the spread of a
chytrid fungus (Batrachochytrium dendrobatidis, Bd), and habitat
modification and destruction, have occurred throughout much of the
northern Mexican gartersnake's U.S. distribution (Nickerson and Mays
1970, p. 495; Vitt and Ohmart 1978, p. 44; Ohmart et al. 1988, p. 150;
Rosen and Schwalbe 1988, Appendix I; 1995, p. 452; 1996, pp. 1-3; 1997,
p. 1; 2002b, pp. 232-238; 2002c, pp. 1, 31; Clarkson and Rorabaugh
1989, pp. 531-538; Sredl et al. 1995a, pp. 7-8; 1995b, pp. 8-9, 1995c,
pp. 7-8; 2000, p. 10; Holm and Lowe 1995, pp. 45-46; Rosen et al.
1996b, p. 2; 2001, pp. 2, 22; Degenhardt et al. 1996, p. 319; Fernandez
and Rosen 1996, pp. 6-20; Drost and Nowak 1997, p. 11; Turner et al.
1999, p. 11; Nowak and Spille 2001, p. 32; Holycross et al. 2006, pp.
13-14, 52-61). Specifically, Holycross et al. (2006, pp. 53-57, 59)
documented potential extirpations of the northern Mexican gartersnake's
native leopard frog prey base at several currently, historically, or
potentially occupied locations, including the Agua Fria River in the
vicinity of Table Mesa Road and Little Grand Canyon Ranch, and at Rock
Springs, Dry Creek from Dugas Road to Little Ash Creek, Little Ash
Creek from Brown Spring to Dry Creek, Sycamore Creek (Agua Fria
[[Page 41516]]
subbasin) in the vicinity of the Forest Service Cabin, the Page Springs
and Bubbling Ponds fish hatchery along Oak Creek, Sycamore Creek (Verde
River subbasin) in the vicinity of the confluence with the Verde River
north of Clarkdale, along several reaches of the Verde River mainstem,
Cherry Creek on the east side of the Sierra Ancha Mountains, and Tonto
Creek from Gisela to ``the Box,'' near its confluence with Rye Creek.
Rosen et al. (2001, p. 22) identified the expansion of bullfrogs
into the Sonoita grasslands, which contain occupied northern Mexican
gartersnake habitat, and the introduction of crayfish into Lewis
Springs, as being of particular concern in terms of future recovery
efforts for the northern Mexican gartersnake. Rosen et al. (1995, pp.
252-253) sampled aquatic herpetofauna at 103 sites in the Chiricahua
Mountains region, which included the Chiricahua, Dragoon, and
Peloncillo mountains, and the Sulphur Springs, San Bernardino, and San
Simon valleys. They found that 43 percent of all cold-blooded aquatic
and semi-aquatic vertebrate species detected were nonnative. The most
commonly encountered nonnative species was the bullfrog (Rosen et al.
1995, p. 254). Witte et al. (2008, p. 1) found that the disappearance
of ranid frog populations in Arizona were 2.6 times more likely in the
presence of crayfish. Witte et al. (2008, p. 7) emphasized the
significant influence of nonnative species on the disappearance of
ranid frogs in Arizona.
In addition to harmful nonnative species, disease and nonnative
parasites have been implicated in the decline of the prey base of the
northern Mexican gartersnake. In particular, the outbreak of
chytridiomycosis or ``Bd,'' a skin fungus, has been identified as a
chief causative agent in the significant declines of many of the native
ranid frogs and other amphibian species. In addition, regional concerns
exist for the native fish community due to nonnative parasites, such as
the Asian tapeworm (Bothriocephalus acheilognathi) in southeastern
Arizona (Rosen and Schwalbe 1997, pp. 14-15; 2002c, pp. 1-19; Morell
1999, pp. 728-732; Sredl and Caldwell 2000, p. 1; Hale 2001, pp. 32-37;
Bradley et al. 2002, p. 206). As indicated, Bd has been implicated in
both large-scale declines and local extirpations of many amphibians,
chiefly anuran species, around the world (Johnson 2006, p. 3011). Lips
et al. (2006, pp. 3166-3169) suggest that the high virulence and large
number of potential hosts make Bd a serious threat to amphibian
diversity. In Arizona, Bd infections have been reported in several of
the native prey species of the northern Mexican gartersnake within the
distribution of the snake (Morell 1999, pp. 731-732; Sredl and Caldwell
2000, p. 1; Hale 2001, pp. 32-37; Bradley et al. 2002, p. 207; USFWS
2002, pp. 40802-40804; USFWS 2007, pp. 26, 29-32). Declines of native
prey species of the northern Mexican gartersnake from Bd infections
have contributed to the decline of this species in the United States
(Morell 1999, pp. 731-732; Sredl and Caldwell 2000, p. 1; Hale 2001,
pp. 32-37; Bradley et al. 2002, p. 207; USFWS 2002, pp. 40802-40804;
USFWS 2007, pp. 26, 29-32). Evidence of Bd-related amphibian declines
has been confirmed in portions of southern Mexico (just outside the
range of northern Mexican gartersnakes), and data suggest declines are
more prevalent at higher elevations (Lips et al. 2004, pp. 560-562).
However, much less is known about the role of Bd in amphibian declines
across much of Mexico, in particular the mountainous regions of Mexico
(including much of the range of northern Mexican gartersnakes in
Mexico) as the region is significantly understudied (Young et al. 2000,
p. 1218). Because narrow-headed gartersnakes feed on fish, Bd has not
affected their prey base. Also, research shows that the fungus
Batrachochytrium can grow on boiled snakeskin (keratin) in the
laboratory (Longcore et al. 1999, p. 227), indicating the potential for
disease outbreaks in wild snake populations if conditions are
favorable; however no observations have been made in the field, and we
found no other data that propose a direct linkage between Bd and snake
mortality.
The Effects of Bullfrogs on Native Aquatic Communities
Bullfrogs are generally considered one of the most serious threats
to northern Mexican gartersnakes throughout their range (Conant 1974,
pp. 471, 487-489; Rosen and Schwalbe 1988, pp. 28-30; Rosen et al.
2001, pp. 21-22). Bullfrogs have and do threaten some populations of
narrow-headed gartersnakes, but differing habitat preferences between
the two temper their effect on narrow-headed gartersnakes. Bullfrogs
adversely affect northern Mexican and narrow-headed gartersnakes
through direct predation of juveniles and sub-adults. Bullfrogs also
compete with northern Mexican gartersnakes. Bullfrogs are not native to
the southwestern United States or Mexico, and first appeared in Arizona
in 1926, as a result of a systematic introduction effort by the State
Game Department (now, the AGFD) for the purposes of sport hunting and
as a food source (Tellman 2002, p. 43). We are not certain when
bullfrogs were first reported from New Mexico but presume it was many
decades ago. Bullfrogs are extremely prolific, are strong colonizers,
and may disperse distances of up to 10 mi (16 km) across uplands, and
likely further within drainages (Bautista 2002, p. 131; Rosen and
Schwalbe 2002a, p. 7; Casper and Hendricks 2005, p. 582; Suhre 2008,
pers. comm.).
Bullfrogs are large-bodied, voracious, opportunistic, even
cannibalistic predators that readily attempt to consume any living
thing smaller than them. Bullfrogs have a highly varied diet, which has
been documented to include vegetation, invertebrates, fish, birds,
mammals, amphibians, and reptiles, including numerous species of snakes
(eight genera, including six different species of gartersnakes, two
species of rattlesnakes, and Sonoran gophersnakes (Pituophis catenifer
affinis)) (Bury and Whelan 1984, p. 5; Clarkson and DeVos 1986, p. 45;
Holm and Lowe 1995, pp. 37-38; Carpenter et al. 2002, p. 130; King et
al. 2002; Hovey and Bergen 2003, pp. 360-361; Casper and Hendricks
2005, pp. 543-544; Combs et al. 2005, p. 439; Wilcox 2005, p. 306;
DaSilva et al. 2007, p. 443; Neils and Bugbee 2007, p. 443; Rowe and
Garcia 2012, pp. 633-634). In one study, three different species of
gartersnakes (Thamnophis sirtalis, T. elegans, and T. ordinoides)
totaling 11 snakes were found inside the stomachs of resident bullfrogs
from a single region (Jancowski and Orchard 2013, p. 26). Bullfrogs can
significantly reduce or eliminate the native amphibian populations
(Moyle 1973, pp. 18-22; Conant 1974, pp. 471, 487-489; Hayes and
Jennings 1986, pp. 491-492; Rosen and Schwalbe 1988, pp. 28-30; 2002b,
pp. 232-238; Rosen et al. 1995, pp. 257-258; 2001, pp. 2, Appendix I;
Wu et al. 2005, p. 668; Pearl et al. 2004, p. 18; Kupferberg 1994, p.
95; Kupferburg 1997, pp. 1736-1751; Lawler et al. 1999; Bury and Whelan
1986, pp. 9-10; Hayes and Jennings 1986, pp. 500-501; Jones and Timmons
2010, pp. 473-474), which are vital for northern Mexican gartersnakes.
Different age classes of bullfrogs within a community can affect native
ranid populations via different mechanisms. Juvenile bullfrogs affect
native ranids through competition, male bullfrogs affect native ranids
through predation, and female bullfrogs affect native ranids through
both mechanisms depending on body size and microhabitat (Wu et al.
2005, p. 668). Pearl et al. (2004, p. 18) also suggested that the
effect of bullfrog introductions on native ranids may be different
based
[[Page 41517]]
on specific habitat conditions, but also suggested that an individual
ranid frog species' physical ability to escape influences the effect of
bullfrogs on each native ranid community.
Bullfrogs have been documented throughout the State of Arizona.
Holycross et al. (2006, pp. 13-14, 52-61) found bullfrogs at 55 percent
of sample sites in the Agua Fria subbasin, 62 percent of sites in the
Verde River subbasin, 25 percent of sites in the Salt River subbasin,
and 22 percent of sites in the Gila River subbasin. In total, bullfrogs
were observed at 22 of the 57 sites surveyed (39 percent) across the
Mogollon Rim (Holycross et al. 2006, p. 13). A number of authors have
also documented the presence of bullfrogs through their survey efforts
throughout many subbasins in Arizona and New Mexico adjacent to the
historical distribution of the northern Mexican or narrow-headed
gartersnake, including northern Arizona (Sredl et al. 1995a, p. 7;
1995c, p. 7), central Arizona and along the Mogollon Rim of Arizona and
New Mexico (Nickerson and Mays 1970, p. 495; Hulse 1973, p. 278; Sredl
et al. 1995b, p. 9; Drost and Nowak 1997, p. 11; Nowak and Spille 2001,
p. 11; Holycross et al. 2006, pp. 15-51; Wallace et al. 2008; pp. 243-
244; Helleckson 2012a, pers. comm.), southern Arizona (Rosen and
Schwalbe 1988, Appendix I; 1995, p. 452; 1996, pp. 1-3; 1997, p. 1;
2002b, pp. 223-227; 2002c, pp. 31, 70; Holm and Lowe 1995, pp. 27-35;
Rosen et al. 1995, p. 254; 1996a, pp. 16-17; 1996b, pp. 8-9; 2001,
Appendix I; Turner et al. 1999, p. 11; Sredl et al. 2000, p. 10; Turner
2007; p. 41), and along the Colorado River (Vitt and Ohmart 1978, p.
44; Clarkson and DeVos 1986, pp. 42-49; Ohmart et al. 1988, p. 143). In
one of the more conspicuous examples, bullfrogs were identified as the
primary cause for collapse of both the northern Mexican gartersnake and
its prey base on the SBNWR (Rosen and Schwalbe 1988, p. 28; 1995, p.
452; 1996, pp. 1-3; 1997, p. 1; 2002b, pp. 223-227; 2002c, pp. 31, 70;
Rosen et al. 1996b, pp. 8-9).
Perhaps one of the most serious consequences of bullfrog
introductions is their persistence in an area once they have become
established, and the subsequent difficulty in eliminating bullfrog
populations. Rosen and Schwalbe (1995, p. 452) experimented with
bullfrog removal at various sites on the SBNWR, in addition to a
control site with no bullfrog removal in similar habitat on the Buenos
Aires National Wildlife Refuge (BANWR). Removal of adult bullfrogs,
without removal of eggs and tadpoles, resulted in a substantial
increase in younger age-class bullfrogs where removal efforts were the
most intensive (Rosen and Schwalbe 1997, p. 6). Contradictory to the
goals of bullfrog eradication, evidence from dissection samples from
young adult and sub-adult bullfrogs indicated these age-classes readily
prey upon juvenile bullfrogs (up to the average adult leopard frog
size) as well as juvenile gartersnakes, which suggests that the
selective removal of only the large adult bullfrogs (presumed to be the
most dangerous size class to leopard frogs and gartersnakes), favoring
the young adult and sub-adult age classes, could indirectly lead to
increased predation of leopard frogs and juvenile gartersnakes (Rosen
and Schwalbe 1997, p. 6). These findings illustrate that in addition to
large adults, subadult bullfrogs also negatively impact northern
Mexican gartersnakes and their prey species. It also indicates the
importance of including egg mass and tadpole removal during efforts to
control bullfrogs and timing removal projects to ensure reproductive
bullfrogs are removed prior to breeding. Some success in regional
bullfrog eradication has been had in a few cases described below in the
section entitled ``Current Conservation of Northern Mexican and Narrow-
headed Gartersnakes.''
Bullfrogs not only compete with the northern Mexican gartersnake
for prey items but directly prey upon juvenile and occasionally sub-
adult northern Mexican and narrow-headed gartersnakes (Rosen and
Schwalbe 1988, pp. 28-31; 1995, p. 452; 2002b, pp. 223-227; Holm and
Lowe 1995, pp. 29-29; Rossman et al. 1996, p. 177; AGFD In Prep., p.
12; 2001, p. 3; Rosen et al. 2001, pp. 10, 21-22; Carpenter et al.
2002, p. 130; Wallace 2002, p. 116). A well-circulated photograph of an
adult bullfrog in the process of consuming a northern Mexican
gartersnake at Parker Canyon Lake, Cochise County, Arizona, taken by
John Carr of the Arizona Game and Fish Department in 1964, provides
photographic documentation of bullfrog predation (Rosen and Schwalbe
1988, p. 29; 1995, p. 452). The most recent, physical evidence of
bullfrog predation of northern Mexican gartersnakes is provided in
photographs of a dissected bullfrog at Pasture 9 Tank in the San Rafael
Valley of Arizona that had a freshly-eaten neonatal northern Mexican
gartersnake in its stomach (Akins 2012, pers. comm.).
A common observation in northern Mexican gartersnake populations
that co-occur with bullfrogs is a preponderance of large, mature adult
snakes with conspicuously low numbers of individuals in the newborn and
juvenile age size classes due to bullfrogs more effectively preying on
young small snakes, which ultimately leads to low reproductive rates
and survival of young (Rosen and Schwalbe 1988, p. 18; Holm and Lowe
1995, p. 34). In lotic (flowing water) systems, bullfrogs prefer sites
with low or limited flow, such as backwaters, side channels, and pool
habitat. These areas are also used frequently by northern Mexican and
narrow-headed gartersnakes, which likely results in increased predation
rates and likely depressed recruitment of gartersnakes. Potential
recruitment problems for northern Mexican gartersnakes due to effects
from nonnative species are suspected at Tonto Creek (Wallace et al.
2008, pp. 243-244). Rosen and Schwalbe (1988, p. 18) stated that the
low recruitment at the SBNWR, a typical characteristic of gartersnake
populations affected by harmful nonnative species, is the likely cause
of that populations' decline and possibly for declines in populations
throughout their range in Arizona. Specific localities within the
distribution of northern Mexican and narrow-headed gartersnakes where
bullfrogs have been detected are presented in Appendix A (available at
http://www.regulations.gov under Docket No. FWS-R2-ES-2013-0071).
The Effects of Crayfish on Native Aquatic Communities
Crayfish are a nonnative species in Arizona and New Mexico and are
a primary threat to many prey species of northern Mexican and narrow-
headed gartersnakes, and may also prey upon juvenile gartersnakes
themselves (Fernandez and Rosen 1996, p. 25; Voeltz 2002, pp. 87-88;
USFWS 2007, p. 22). Fernandez and Rosen (1996, p. 3) studied the
effects of crayfish introductions on two stream communities in Arizona,
a low-elevation semi-desert stream and a high mountain stream, and
concluded that crayfish can noticeably reduce species diversity and
destabilize food chains in riparian and aquatic ecosystems through
their effect on vegetative structure, stream substrate (stream bottom;
i.e., silt, sand, cobble, boulder) composition, and predation on eggs,
larval, and adult forms of native invertebrate and vertebrate species.
Crayfish fed on embryos, tadpoles, newly metamorphosed frogs, and adult
leopard frogs, but they did not feed on egg masses (Fernandez and Rosen
1996, p. 25). However, Gamradt and Kats (1996, p. 1155) found that
crayfish readily consumed the egg masses of California newts (Taricha
torosa). Crayfish are known to also eat fish eggs and larva (Inman et
al. 1998, p. 17), especially those bound to the substrate (Dorn and
[[Page 41518]]
Mittlebach 2004, p. 2135). Fernandez and Rosen (1996, pp. 6-19, 52-56)
and Rosen (1987, p. 5) discussed observations of inverse relationships
between crayfish abundance and native reptile and amphibian
populations, including narrow-headed gartersnakes, northern leopard
frogs, and Chiricahua leopard frogs. Crayfish may also affect native
fish populations. Carpenter (2005, pp. 338-340) documented that
crayfish may reduce the growth rates of native fish through competition
for food and noted that the significance of this impact may vary
between species.
Crayfish alter the abundance and structure of aquatic vegetation by
grazing on aquatic and semiaquatic vegetation, which reduces the cover
needed by frogs and gartersnakes, as well as the food supply for prey
species such as tadpoles (Fernandez and Rosen 1996, pp. 10-12).
Fernandez and Rosen (1996, pp. 10-12) found that crayfish frequently
burrow into stream banks, leading to increased bank erosion, stream
turbidity, and siltation of stream bottoms. Creed (1994, p. 2098) found
that filamentous alga (Cladophora glomerata) was at least 10-fold
greater in aquatic habitats that lacked crayfish. Filamentous alga is
an important component of aquatic vegetation that provides cover for
foraging gartersnakes, as well as microhabitat for prey species.
Crayfish have recently been found to also act as a host for the
amphibian disease-causing fungus, Bd (McMahon et al. (2013, pp. 210-
213). This could have serious implications for northern Mexican
gartersnakes because crayfish can now be considered a source of disease
in habitat that is devoid of amphibians but otherwise potentially
suitable habitat for immigrating amphibians, such as leopard frogs,
which could serve as a prey base. Because crayfish are so widespread
throughout Arizona, New Mexico, and portions of Mexico, this could have
broad, negative implications for the recovery of native leopard frogs,
and therefore the recovery of northern Mexican gartersnakes.
Inman et al. (1998, p. 3) documented crayfish as widely distributed
and locally abundant in a broad array of natural and artificial free-
flowing and still-water habitats throughout Arizona, many of which
overlap the historical and current distribution of northern Mexican and
narrow-headed gartersnakes. Hyatt (undated, p. 71) concluded that the
majority of waters in Arizona contained at least one species of
crayfish. In surveying for northern Mexican and narrow-headed
gartersnakes, Holycross et al. (2006, p. 14) found crayfish in 64
percent of the sample sites in the Agua Fria subbasin; in 85 percent of
the sites in the Verde River subbasin; in 46 percent of the sites in
the Salt River subbasin; and in 67 percent of the sites in the Gila
River subbasin. In total, crayfish were observed at 35 (61 percent) of
the 57 sites surveyed across the Mogollon Rim (Holycross et al. 2006,
p. 14), most of which were sites historically or currently occupied by
northern Mexican or narrow-headed gartersnakes, or sites the
investigators believed possessed suitable habitat and may be occupied
by these gartersnakes based upon the their known historical
distributions.
A number of authors have documented the presence of crayfish
through their survey efforts throughout Arizona and New Mexico in
specific regional areas, drainages, and lentic wetlands within or
adjacent to the historical distribution of the northern Mexican or
narrow-headed gartersnake, including northern Arizona (Sredl et al.
1995a, p. 7; 1995c, p. 7), central Arizona and along the Mogollon Rim
of Arizona and New Mexico (Sredl et al. 1995b, p. 9; Fernandez and
Rosen 1996, pp. 54-55, 71; Inman et al. 1998, Appendix B; Nowak and
Spille 2001, p. 33; Holycross et al. 2006, pp. 15-51; Brennan 2007, p.
7; Burger 2008, p. 4; Wallace et al. 2008; pp. 243-244; Brennan and
Rosen 2009, p. 9; Karam et al. 2009; pp. 2-3; Helleckson 2012a, pers.
comm.), southern Arizona (Rosen and Schwalbe 1988, Appendix I; Inman et
al. 1998, Appendix B; Sredl et al. 2000, p. 10; Rosen et al. 2001,
Appendix I), and along the Colorado River (Ohmart et al. 1988, p. 150;
Inman et al. 1998, Appendix B). Specific localities within the
distribution of northern Mexican and narrow-headed gartersnakes where
crayfish have been detected are presented in Appendix A (available at
http://www.regulations.gov under Docket No. FWS-R2-ES-2013-0071).
Like bullfrogs, crayfish can be very difficult, if not impossible,
to eradicate once they have become established in an area, depending on
the complexity of the habitat (Rosen and Schwalbe 1996a, pp. 5-8;
2002a, p. 7; Hyatt undated, pp. 63-71). The use of biological control
agents such as bacteria, nematodes, and viruses were explored in
addressing the invasion and persistence of crayfish in the southwestern
United States, using the organisms' cannibalistic nature as a vector
(Davidson et al. 2010, pp. 297-310). The use of biological control
agents tested found them to be ineffective or infeasible in controlling
crayfish, but a number of other biological pathogens have been
described in freshwater crayfish that may lend promise to finding an
appropriate control agent in the future (Davidson et al. 2010, pp. 307-
308). In addition, recent experimentation with ammonia as a piscicide
indirectly found that crayfish were also effectively eradicated in
field trials; the first successful and most promising control method
for this harmful nonnative species in recent times (Ward et al. 2013,
pp. 402-404). However, it could be potentially several years before
ammonia is licensed for such use, if ever.
The Effects of Predation-Related Injuries to Gartersnakes
The tails of gartersnakes are often broken off during predation
attempts by bullfrogs or crayfish and do not regenerate. The incidence
of tail breaks in gartersnakes can often be used to assess predation
pressure within gartersnake populations. Attempted predation occurs on
both sexes and all ages of gartersnakes within a population, although
some general trends have been detected. For example, female
gartersnakes may be more susceptible to predation as evidenced by the
incidence of tail damage (Willis et al. 1982, pp. 100-101; Rosen and
Schwalbe1988, p. 22; Mushinsky and Miller 1993, pp. 662-664; Fitch
2003, p. 212). This can be explained by higher basking rates associated
with pregnant females that increase their visibility to predators.
Fitch (2003, p. 212) found that tail injuries in the common gartersnake
occurred more frequently in adults than in juveniles. Predation on
juvenile snakes likely results in complete consumption of the animal,
which would limit observations of tail injury in their age class.
Tail injuries can have negative effects on the health, longevity,
and overall success of individual gartersnakes from infection, slower
swimming and crawling speeds, or impeding reproduction. Mushinsky and
Miller (1993, pp. 662-664) commented that, while tail breakage in
gartersnakes can save the life of an individual snake, it also leads to
permanent handicapping of the snake, resulting in slower swimming and
crawling speeds, which could leave the snake more vulnerable to
predation or affect its foraging ability. Willis et al. (1982, p. 98)
discussed the incidence of tail injury in three species in the genus
Thamnophis (common gartersnake, Butler's gartersnake (T. butleri), and
the eastern ribbon snake (T. sauritus)) and concluded that individuals
that suffered nonfatal injuries prior to reaching a length of 12 in (30
cm) are not likely to survive and that physiological stress during
post-injury hibernation may play an important role in subsequent
[[Page 41519]]
mortality. While northern Mexican or narrow-headed gartersnakes may
survive an individual predation attempt from a bullfrog or crayfish
with tail damage, secondary effects from infection of the wound may
significantly contribute to mortality of individuals. Perry-Richardson
et al. (1990, p. 77) described the importance of tail-tip alignment in
the successful courtship and mating in Thamnophiine snakes and found
that missing or shortened tails adversely affected these activities
and, therefore, mating success. In researching the role of tail length
in mating success in the red-sided gartersnake (Thamnophis sirtalis
parietalis), Shine et al. (1999, p. 2150) found that males that
experienced injuries or the partial or whole loss of the tail
experienced a three-fold decrease in mating success.
The frequency of tail injuries can be quite high in a given
gartersnake population; for example at the SBNWR (Rosen and Schwalbe
1988, pp. 28-31), 78 percent of northern Mexican gartersnakes had
broken tails with a ``soft and club-like'' terminus, which suggests
repeated injury from multiple predation attempts by bullfrogs. While
medically examining pregnant female northern Mexican gartersnakes,
Rosen and Schwalbe (1988, p. 28) noted bleeding from the posterior
region, which suggested to the investigators the snakes suffered from
``squeeze-type'' injuries inflicted by adult bullfrogs. In another
example, Holm and Lowe (1995, pp. 33-34) observed tail injuries in 89
percent of northern Mexican gartersnakes during the early 1990s in
Scotia Canyon in the Huachuca Mountains, as well as a skewed age class
ration that favored adults over subadults, which is consistent with
data collected by Willis et al. (1982, pp. 100-101) on other
gartersnake species. Bullfrogs are largely thought to be responsible
for the significant decline of northern Mexican gartersnake and its
prey base at this locality, although the latter has improved through
recovery actions. In the Black River, crayfish are very abundant and
have been identified as the likely cause for a high-frequency of tail
injuries to narrow-headed gartersnakes (Brennan 2007, p. 7; Brennan and
Rosen 2009, p. 9). Brennan (2007, p. 5) found that in the Black River,
14 of 15 narrow-headed gartersnakes captured showed evidence of damaged
or missing tails (Brennan 2007, p. 5). In 2009, 16 of 19 narrow-headed
gartersnakes captured in the Black River showed evidence of damaged or
missing tails (Brennan and Rosen 2009, p. 8). In the upper Verde River
region, Emmons and Nowak (2013, p. 5) reported that 18 of 49 (37
percent) northern Mexican gartersnakes captured had scars (n = 17) and/
or missing tails tips (n = 7).
Vegetation or other forms of protective cover may be particularly
important for gartersnakes to reduce the effects of harmful nonnative
species on populations. For example, the population of northern Mexican
gartersnakes at the Page Springs and Bubbling Ponds State Fish
Hatcheries occurs with harmful nonnative species (Boyarski 2008b, pp.
3-4, 8). Yet, only 11 percent of northern Mexican gartersnakes captured
in 2007 were observed as having some level of tail damage (Boyarski
2008b, pp. 5, 8). The relatively low occurrence of tail damage, as
compared to 78 percent of snakes with tail damage found by Rosen and
Schwalbe (1988, pp. 28-31), may indicate: (1) Adequate vegetation
density was used by gartersnakes to avoid harmful nonnative species
predation attempts; (2) a relatively small population of harmful
nonnative species may be at a comparatively lower density than sites
sampled by previous studies (harmful nonnative species population
density data were not collected by Boyarski (2008b)); (3) gartersnakes
may not have needed to move significant distances at this locality to
achieve foraging success, which might reduce the potential for
encounters with harmful nonnative species; or (4) gartersnakes
infrequently escaped predation attempts by harmful nonnative species,
were removed from the population, and were consequently not detected by
surveys.
The Expansion of the American Bullfrog and Crayfish in Mexico
Bullfrogs have recently been documented as a significant threat to
native aquatic and riparian species throughout Mexico. Luja and
Rodr[iacute]guez-Estrella (2008, pp. 17-22) examined the invasion of
the bullfrog in Mexico. The earliest records of bullfrogs in Mexico
were Nuevo Leon (1853), Tamaulipas (1898), Morelos (1968), and Sinaloa
(1969) (Luja and Rodr[iacute]guez-Estrella 2008, p. 20). By 1976, the
bullfrog was documented in seven more states: Aguacalientes, Baja
California Sur, Chihuahua, Distrito Federal, Puebla, San Luis Potosi,
and Sonora (Luja and Rodr[iacute]guez-Estrella 2008, p. 20). The
bullfrog was recently verified from the state of Hidalgo, Mexico, at an
elevation of 8,970 feet (2,734 m), which indicates the species
continues to spread in that country and can exist even at the uppermost
elevations inhabited by northern Mexican gartersnakes (Duifhuis Rivera
et al. 2008, p. 479). As of 2008, Luja and Rodr[iacute]guez-Estrella
(2008, p. 20) have recorded bullfrogs in 20 of the 31 Mexican States
(65 percent of the states in Mexico) and suspect that they have invaded
other States, but were unable to find documentation.
Sponsored by the then Mexican Secretary of Aquaculture Support,
bullfrogs have been commercially produced for food in Mexico in
Yucatan, Nayarit, Morelos, Estado de Mexico, Michoac[aacute]n,
Guadalajara, San Luis Potosi, Tamaulipas, and Sonora (Luja and
Rodr[iacute]guez-Estrella 2008, p. 20). However, frog legs ultimately
never gained popularity in Mexican culinary culture (Conant 1974, pp.
487-489), and Luja and Rodr[iacute]guez-Estrella (2008, p. 22) point
out that only 10 percent of these farms remain in production. Luja and
Rodr[iacute]guez-Estrella (2008, pp. 20, 22) document instances where
bullfrogs have escaped production farms and suspect the majority of the
frogs that were produced commercially in farms that have since ceased
operation have assimilated into surrounding habitat.
Luja and Rodr[iacute]guez-Estrella (2008, p. 20) also state that
Mexican people deliberately introduce bullfrogs for ornamental
purposes, or ``for the simple pleasure of having them in ponds.'' The
act of deliberately releasing bullfrogs into the wild in Mexico was
cited by Luja and Rodr[iacute]guez-Estrella (2008, p. 21) as being
``more common than we can imagine.'' Bullfrogs are available for
purchase at some Mexican pet stores (Luja and Rodr[iacute]guez-Estrella
2008, p. 22). Luja and Rodr[iacute]guez-Estrella (2008, p. 21) state
that bullfrog eradication efforts in Mexico are often thwarted by their
popularity in rural communities (presumably as a food source).
Currently, no regulation exists in Mexico to address the threat of
bullfrog invasions or prevent their release into the wild (Luja and
Rodr[iacute]guez-Estrella 2008, p. 22).
Rosen and Melendez (2006, p. 54) report bullfrog invasions to be
prevalent in northwestern Chihuahua and northwestern Sonora, where the
northern Mexican gartersnake is thought to occur. In many areas, native
leopard frogs were completely displaced where bullfrogs were observed.
Rosen and Melendez (2006, p. 54) also demonstrated the relationship
between fish and amphibian communities in Sonora and western Chihuahua.
Native leopard frogs, a primary prey item for the northern Mexican
gartersnake, only occurred in the absence of nonnative fish, and were
absent from waters containing nonnative species, which included several
major waters. In Sonora, Rorabaugh (2008a, p. 25) also
[[Page 41520]]
considers the bullfrog to be a significant threat to the northern
Mexican gartersnake and its prey base, substantiated by field
observations made during surveys conducted in Chihuahua and Sonora in
2006 (Rorabaugh 2008b, p. 1).
Few data were found on the presence or distribution of nonnative
crayfish species in Mexico. However, in a 2-week gartersnake survey
effort in 2006 in northern Mexico, crayfish were observed as ``widely
distributed'' in the valleys of western Chihuahua (Rorabaugh 2008b, p.
1). Based on the invasive nature of crayfish ecology and their
distribution in the United States along the Border region, it is
reasonable to assume that, at a minimum, crayfish are likely
distributed along the entire Border region of northern Mexico, adjacent
to where they occur in the United States.
Risks to Gartersnakes From Fisheries Management Activities
The decline in native fish communities from the effects of harmful
nonnative fish species has spurred resource managers to take action to
help recover native fish species. While we fully support activities
designed to help recover native fish, recovery actions for native fish,
in the absence of thorough planning, can have significant adverse
effects on resident gartersnake populations.
Piscicides--Piscicide is a term that refers to a ``fish poison.''
The use of piscicides, such as rotenone or antimycin A, for the removal
of harmful nonnative fish species has widely been considered invaluable
for the conservation and recovery of imperiled native fish species
throughout the United States, and in particular the Gila River basin of
Arizona and New Mexico (Dawson and Kolar 2003, entire). Antimycin A is
rarely used anymore, and has been largely replaced by rotenone in field
applications. Experimentation with ammonia as a piscicide has shown
promising results and may ultimately replace rotenone in the future as
a desired control method if legally registered for such use (Ward et
al. 2013, pp. 402-404). Currently, rotenone is the most commonly used
piscicide. The active ingredient in rotenone is a natural chemical
compound extracted from the stems and roots of tropical plants in the
family Leguminosae that interrupts oxygen absorption in gill-breathing
animals (Fontenot et al. 1994, pp. 150-151). In the greater Gila River
subbasin alone, 57 streams or water bodies have been treated with
piscicide, some on several occasions spanning many years (Carpenter and
Terrell 2005; Table 6). However, this practice has been the source of
recent controversy due to a perceived link between rotenone and
Parkinson's disease in humans, as well as potential effects to
livestock. Speculation of the potential role of rotenone in Parkinson's
disease was fueled by Tanner et al. (2011, entire) which correlated the
incidence of the disease with lifetime exposure to certain pesticides,
including rotenone. As a result, in 2012, the Arizona State Legislature
proposed two bills that called for the development of an environmental
impact statement prior to the application of rotenone or antimycin A
(S.B. 1453, see State of Arizona Senate (2012b)) and urged the U.S.
Environmental Protection Agency to deregister rotenone from use in the
United States (S.B. 1009, see State of Arizona Senate (2012b)). Public
safety considerations were fully evaluated by a multi-disciplined
technical team of specialists that found no correlation between
rotenone applications performed, according to product label
instructions, and Parkinson's disease (Rotenone Review Advisory
Committee 2012, pp. 24-25). Nonetheless, continued anxiety regarding
the use of piscicides for conservation and management of fish
communities leaves an uncertain future for this invaluable management
tool. Should circumstances result in the discontinued practice of using
piscicides for fish recovery and management, the likelihood of recovery
for listed or sensitive aquatic vertebrates in Arizona, such as
northern Mexican and narrow-headed gartersnakes, would be substantially
reduced, if not eliminated outright.
We are supportive of the use of piscicides and consider the
practice a vital and scientifically sound tool, the only tool in most
circumstances, for reestablishing native fish communities and removing
threats related to nonnative aquatic species in occupied northern
Mexican and narrow-headed gartersnake habitat. However, it is equally
important that effects of such treatments to these gartersnakes be
evaluated during the project planning phase, specifically the amount of
time a treated water body remains fishless post-treatment. The time
period between rotenone applications and the subsequent restocking of
native fish is contingent on two basic variables, the time it takes for
piscicide levels to reach nontoxic levels and the level of certainty
required to ensure that renovation goals and objectives have been met
prior to restocking. Implementation of the latter consideration may
vary from weeks, to months, to a year or longer, depending on the level
of certainty required by project proponents. Carpenter and Terrell
(2005, p. 14) reported that standard protocols, used by the Arizona
Game and Fish Department for Apache trout renovations, required two
applications of piscicide before repatriating native fish to a stream,
waiting a season to see if the renovation was successful, and then
continuing to renovate if necessary. Another recommendation of past
protocols included a goal for the renovated water body to remain
fishless an entire year before restocking (Carpenter and Terrell 2005,
p. 14). At a minimum and according to our files, reaches of Big Bonito
Creek, the West Fork Black River, West Fork Gila River, Iron Creek,
Little Creek, Black Canyon, and O'Donnell Creek have all been subject
to fish renovations using these or similarly accepted protocols
(Carpenter and Terrell 2005; Table 6; Paroz and Probst 2009, p. 4;
Hellekson 2012a, pers. comm.). Therefore, northern Mexican or narrow-
headed gartersnake populations in these streams have likely been
adversely affected, due to the eradication of a portion of, or their
entire, prey base in these systems for varying periods of time. Big
Bonito Creek was restocked with salvaged native fish shortly after
renovation occurred. However, we are uncertain how long other stream
reaches remained fishless post-treatment, but presume a minimum of
weeks in each instance, and possibly a year or longer in some
instances.
Future planning in fisheries management has identified several
streams within the distribution of narrow-headed gartersnakes in New
Mexico for potential fish barrier construction, for which piscicide
applications are likely necessary. These streams include Little Creek,
West Fork Gila River, Middle Fork Gila River, Turkey Creek, Saliz
Creek, Dry Blue Creek, and the San Francisco River (Riley and Clarkson
2005, pp. 4-5, 7, 9, 12; Clarkson and Marsh 2012, p. 8; 2013, pp. 1, 4,
6). Of these, the Middle Fork Gila River and Turkey Creek appear to the
most likely-chosen for renovation (Clarkson and Marsh 2013, p. 8). Mule
Creek and Cienega Creek, both occupied by northern Mexican
gartersnakes, as well as Whitewater Creek (occupied by narrow-headed
gartersnakes) are under consideration but ultimately may not be chosen
for renovation for undisclosed reasons (Clarkson and Marsh 2013, pp. 8-
9).
In addition to fish, rotenone is toxic to amphibians in their gill-
breathing,
[[Page 41521]]
larval life stages; adult forms tend to avoid treated water (Fontenot
et al. 1994, pp. 151-152). Rotenone has not been found to be directly
toxic to aquatic snakes, but Fontenot et al. (1994, p. 152) suggested
that effects from ingesting affected fish, frogs, or tadpoles may
occur, but have not been adequately researched. The current standard
operating procedures for piscicide application, as adopted nationally
and provided in Finlayson et al. (2010, p. 23), provide guidance for
assuring that non-target, baseline environmental conditions (the biotic
community) are accounted for in assessing whether mitigation measures
are necessary. This procedural protocol states, ``Survival and recovery
of the aquatic community may be demonstrated by sampling plankton,
macroinvertebrates (aquatic insects, crustacea, leeches, and mollusks),
and amphibians (frogs, tadpoles, and larval and adult salamanders)''
(Finlayson et al. 2010, p. 23). This protocol, adopted by the Arizona
Game and Fish Department (see AGFD 2012), does not consider the effects
of leaving a treated water body without a prey base for a sensitive
species, such as the narrow-headed gartersnake, for extended periods of
time. In fact, considerations for non-target aquatic reptiles, in
general, are not mentioned anywhere in this broadly applied piscicide
application protocol. Consequently, we have no reason to assume that
effects to either northern Mexican or narrow-headed gartersnake
populations from the partial or whole-scale removal of their prey base
have been historically considered in piscicide applications, at least
through 2006.
The potentially significant effects to northern Mexican or narrow-
headed gartersnakes described above pertaining to piscicide application
are largely historical in nature in Arizona, and new methodologies have
been developed in Arizona to prevent adverse effects to gartersnake
populations. As of 2012, a new policy was finalized by the Arizona Game
and Fish Department that includes an early and widespread public
notification and planning process that involves the approval of several
decision-makers within four major stages: (1) Piscicide project
internal review and approval; (2) preliminary planning and public
involvement; (3) intermediate planning and public involvement; and (4)
project implementation and evaluation (AGFD 2012, p. 3). Within the
Internal Review and Approval stage of the process, sensitive, endemic,
and listed species potentially impacted by the project must be
identified (AGFD 2012, p. 13), such as northern Mexican or narrow-
headed gartersnakes. In addition, the Arizona Game and Fish Department,
through their Conservation and Mitigation Program developed as part of
their sport fish stocking program through 2021, has committed to
quickly restocking renovated streams that are occupied by either
northern Mexican or narrow-headed gartersnakes (USFWS 2011, Appendix
C).
Although significant efforts are generally made to salvage as many
native fish as possible prior to treatment, logistics of holding fish
for several weeks prior to restocking limit the number of individuals
that can be held safely. Therefore, not every individual fish is
salvaged, and native fish remaining in the stream are subsequently lost
during the treatment. The number of fish subsequently restocked is,
therefore, smaller than the number of fish that were present prior to
the treatment. The full restoration of native fish populations to pre-
treatment levels may take several years, depending on the size of the
treated area and the size and maturity of the founding populations.
Restocking salvaged fish in the fall may allow natural spawning and
recruitment to begin in the spring, which would provide a more
immediate benefit to resident gartersnake populations. With regard to
New Mexico and Mexico, we are uncertain what measures have been
considered in the past, or implemented currently, to prevent
significant adverse impacts to northern Mexican or narrow-headed
gartersnakes from piscicide applications.
Mechanical Methods--In addition to chemical renovation techniques,
mechanical methods using electroshocking equipment are often used in
fisheries management, both for nonnative aquatic species removal and
fisheries survey and monitoring activities that often occur in
conjunction with piscicide treatments. Northern Mexican and narrow-
headed gartersnakes often flee into the water as a first line of
defense when startled. In occupied habitat, gartersnakes present within
the water are often temporarily paralyzed from electrical impulses
intended for fish, and are, therefore, readily detected by surveyors
(Hellekson 2012a, pers. comm.). We are not aware of any research that
has investigated potential short- or long-term consequences of such
electrocutions to gartersnakes. In addition to the occupied streams
noted above that have received piscicide applications (and therefore
received electroshock surveys), Hellekson (2012, pers. comm.) reported
narrow-headed gartersnakes being detected via electroshocking in the
mainstem Gila River from Cliff Dwellings to Little Creek, the East Fork
Gila River, Little Creek, Black Canyon, the Tularosa River, and Dry
Blue Creek. Pettinger and Yori (2011, p. 11) reported detecting two
narrow-headed gartersnakes as a result of electroshocking in the West
Fork Gila River. Thus, electroshock surveys may be a source of
additional data related to the occurrence and distribution of both
northern Mexican and narrow-headed gartersnakes.
Trapping methods are also used in fisheries surveys, for other
applications in aquatic species management, and for the collection of
live baitfish in recreational fishing. One such common method to study
aquatic or semi-aquatic wildlife (including populations of aquatic
snakes such as gartersnakes) is through the use of self-baiting wire
minnow traps. When used to monitor gartersnake populations, wire minnow
traps are anchored to vegetation, logs, etc., along the shoreline (in
most applications) and positioned so that half to one-third of the
trap, along its lateral line, is above water surface to allow snakes to
surface for air. These traps are then checked according to a
predetermined schedule. Because the wire, twine, etc., used to anchor
these traps is fixed in length, these traps may become fully submerged
if there is a sudden, unanticipated rise in water levels (e.g., storm
event). During the monsoon in Arizona and New Mexico, these types of
storm events are common and river hydrographs respond accordingly with
rapid and dynamic increases in flow. We are aware of examples where
northern Mexican gartersnakes, intentionally captured in minnow traps,
have drowned as a direct result of a rapid, unexpected rise in water
levels. Some examples include an adult female northern Mexican
gartersnake along lower Tonto Creek in 2004, and an adult and two
neonates at the Bubbling Springs Hatchery in 2009 and 2010,
respectively (Holycross et al. 2006, p. 41, Boyarski 2011, pp. 2-3). In
another example, involving an underwater funnel trap used to survey for
lowland leopard frogs, a large adult female northern Mexican
gartersnake was discovered deceased in the trap (T. Jones 2012a, pers.
comm.). Death of that individual was likely due to drowning or
predation by numerous crayfish that were also confined in the funnel
trap with the gartersnake (T. Jones 2012a, pers. comm.). There are
likely additional cases where northern Mexican or narrow-headed
gartersnake
[[Page 41522]]
mortality from trapping have not been reported, where trapping has
occurred in occupied habitat prone to flash flooding.
Minnow traps are often deployed for monitoring fully aquatic
species, such as fish, and are, therefore, intentionally positioned in
the water column where they are fully under water. Traps used for this
purpose may be checked less frequently, because risks to fully aquatic
species are less if held in the trap for longer periods of time. As
fish collectively become trapped, the trap becomes incidentally self-
baited for gartersnakes and, if deployed in habitat occupied by either
northern Mexican or narrow-headed gartersnakes, these traps may
accidentally attract, capture, and drown gartersnakes that are actively
foraging under water and are lured to the traps because of captured
prey species. Neonatal northern Mexican and narrow-headed gartersnakes
can also wriggle through the mesh of some wire minnow traps and become
lodged halfway through, depending on the pore size of the wire mesh
(Jaeger 2012, pers. comm.). If not found in time, this situation would
likely result in their death from drowning, predation, or exposure.
The use of minnow traps is also allowed in recreational fishing in
Arizona and New Mexico (AGFD 2013, p. 57; NMDGF 2013, p. 17). In
Arizona and New Mexico, it is lawful to set minnow traps for the
collection of live baitfish (AGFD 2013, pp. 56-57; NMDGF 2013, p. 17).
In Arizona, minnow traps used for collecting live baitfish must be
checked once daily (AGFD 2013, pp. 56-57); in New Mexico, there is no
stipulation on time intervals in the regulations to check minnow traps
(NMDGF 2013, p. 17). In either scenario in either state, these minnow
traps are likely to be fully submerged when in use and pose a drowning
hazard to resident gartersnakes while foraging underwater, as they can
be lured into the traps by fish already caught.
The extent to which trapping-related mortality can affect northern
Mexican or narrow-headed gartersnake populations is uncertain, but
there is reason for concern if adult females are lost from populations
where recruitment appears low or nonexistent, especially in low-density
populations. While we are less certain about northern Mexican or
narrow-headed gartersnake mortality from trapping efforts intended for
other species, we assume such events have historically been unreported,
but also acknowledge that the percentage of snakes intentionally caught
in minnow traps that actually drown is likely to be comparatively low.
We also note that the aquatic community data generated from field
research using these traps are critical to our understanding of
northern Mexican and narrow-headed gartersnake ecology, population
trends, and responses to threats on the landscape, and we believe that
better communication and coordination among programs with regard to
gartersnake concerns can help.
Intentional Dewatering--Lastly, dewatering or water fluctuation
techniques are sometimes considered for eliminating undesirable fish
species from water bodies (Finlayson et al. 2010, p. 4). Dewatering of
occupied northern Mexican or narrow-headed gartersnake habitat would
have obvious deleterious effects to affected populations by removing a
primary habitat feature and eliminating the prey base. Depending on the
availability of suitable habitat regionally and the length of time
water is absent, these activities may ultimately cause local
extirpations of gartersnake populations. Because northern Mexican
gartersnakes often occupy lentic water bodies or intermittently watered
canyon bottoms, where this practice is most feasible, effects of
dewatering activities may disproportionately affect that species. This
technique is being considered by the AGFD for pools within Redrock
Canyon where northern Mexican gartersnakes could be adversely affected;
however it is expected that northern Mexican gartersnakes are being
considered by the AGFD in their implementation planning process.
Summary
In our review of the scientific and commercial literature, we have
found that over time, native aquatic communities, specifically the
native prey bases for northern Mexican and narrow-headed gartersnakes,
have been significantly weakened to the point of near collapse as a
result of the cumulative effects of disease and harmful nonnative
species such as bullfrogs, crayfish, and spiny-rayed fish. Harmful
nonnative species have been intentionally introduced or have naturally
moved into virtually every subbasin throughout the distribution of
northern Mexican and narrow-headed gartersnakes in the United States
and Mexico. According to Geographic Information System GIS analyses,
nonnative, spiny-rayed fish are known to occur in 90 percent of the
historical distribution of the northern Mexican gartersnake and 85
percent of the historical distribution of the narrow-headed gartersnake
in the United States. Bullfrogs are known to occur in 85 percent of the
historical distribution of the northern Mexican gartersnake and 53
percent of the historical distribution of the narrow-headed gartersnake
in the United States. Crayfish are known to occur in 77 percent of the
historical distribution of the northern Mexican gartersnake and 75
percent of the historical distribution of the narrow-headed gartersnake
in the United States. Nonnative, spiny-rayed fish, bullfrogs, and
crayfish are known to occur simultaneously in 65 percent of the
historical distribution of the northern Mexican gartersnake and 44
percent of the historical distribution of the narrow-headed gartersnake
in the United States.
Native fish are important prey for northern Mexican gartersnakes
but much more so for narrow-headed gartersnakes. Predation by and
competition with primarily nonnative, spiny-rayed fish species, and
secondarily with crayfish, are widely considered to be the primary
reason for major declines in native fish communities throughout the
range of both gartersnakes. This fundamental premise is captured by the
fact that in Arizona, 19 of 31 (61 percent) of all native fish species
are listed under the Act. Consequently, Arizona ranks the highest of
all 50 States in the percentage of native fish species with declining
trends (85.7 percent). Similar trends in the loss of native fish
biodiversity have been described in New Mexico and Mexico. Native
amphibians such as the Chiricahua leopard frog, an important component
of the northern Mexican gartersnake prey base, have declined
significantly and may face future declines as a result of Bd and
harmful nonnative species. We cite numerous examples where historical
native frog populations have been wholly replaced by harmful nonnative
species, both on local and regional scales. These declines have
directly contributed to subsequent northern Mexican gartersnake
population declines or extirpations in these areas. Collectively, the
literature confirms that an adequate native prey base is essential to
the conservation and recovery of northern Mexican gartersnakes, and
that this native ranid frog prey base may face an uncertain future if
harmful nonnative species continue to persist and expand their
distributions in occupied habitat.
We have found that the best available commercial and scientific
information supports the fact that harmful nonnative species are the
single most important threat to northern Mexican and narrow-headed
gartersnakes and their prey bases, and therefore have had a profound
role in their decline. A large body of literature documents that
[[Page 41523]]
northern Mexican and narrow-headed gartersnakes are uniquely
susceptible to the influence of harmful nonnative species in their
biotic communities. This sensitivity is largely the result of complex
ecological interactions that result in direct predation on
gartersnakes; shifts in biotic community structure from largely native
to largely nonnative; and competition for a diminished prey base that
can ultimately result in the injury, starvation, or death of northern
Mexican or narrow-headed gartersnakes followed by reduced recruitment,
population declines, and extirpations.
Lastly, we found that fisheries management activities can have
significant negative effects on resident gartersnake populations when
gartersnakes are not considered in project planning and implementation.
We fully support the continued use of rotenone and other fisheries
management techniques in the conservation and recovery of native fish.
However, we also acknowledge the potential and significant threat
rotenone use may pose to these gartersnakes if their habitat is left
with a fish community that is dangerously depleted or entirely removed
for extended periods of time. New policies and mitigation measures have
been developed in Arizona that will reduce the likelihood of these
activities having significant effects on either northern Mexican or
narrow-headed gartersnake populations. However, some level of effect
should still be expected, based on logistical complications and
complexities of restoring fish populations to pre-treatment levels. We
expect to coordinate with resource managers in New Mexico as we do in
Arizona, to ensure gartersnake populations are not significantly
affected by these activities. Other mechanisms or activities used in
fisheries management, such as electroshocking, trapping, or dewatering,
can result in the injury or death of northern Mexican or narrow-headed
gartersnakes, where these activities coincide with extant populations,
and if they have not been considered in the planning or implementation
processes. The significance of these losses depends on the status of
the gartersnake population affected. We found no evidence to conclude
that fisheries management techniques threaten the northern Mexican
gartersnake in Mexico.
On the most basic level, the presence of harmful nonnative species
ultimately affects where northern Mexican and narrow-headed
gartersnakes can live as viable populations. Collectively, the
ubiquitous presence of harmful nonnative species across the landscape
has appreciably reduced the quantity of suitable gartersnake habitat
and changed its spatial orientation on the landscape. Most northern
Mexican and narrow-headed gartersnake populations, even some considered
viable today, live in the presence of harmful nonnative species. While
they continue to persist, they do so under constant stress from
unnatural levels of predation and competition associated with harmful
nonnative species. This weakens their resistance to other threats,
including those that affect the physical suitability of their habitat
(discussed below). This ultimately renders populations much less
resilient to stochastic, natural, or anthropogenic stressors that could
otherwise be withstood. Over time and space, subsequent population
declines have threatened the genetic representation of each species
because many populations have become disconnected and isolated from
neighboring populations. Expanding distances between extant populations
coupled with increasing populations of harmful nonnative species
prevents normal colonizing mechanisms that would otherwise reestablish
populations where they have become extirpated. This subsequently leads
to a reduction in species redundancy when isolated, small populations
are at increased vulnerability to the effects of stochastic events,
without a means for natural recolonization. Ultimately, the effect of
scattered, small, and disjunct populations, without the means to
naturally recolonize, is weakened species resiliency as a whole, which
ultimately enhances the risk of either or both species becoming
endangered. Therefore, based on the best available scientific and
commercial information, we conclude that harmful nonnative species are
the most significant threat to both the northern Mexican and narrow-
headed gartersnake, rangewide, now and in the foreseeable future.
Main Factors That Destroy or Modify the Physical Habitat of Northern
Mexican and Narrow-Headed Gartersnakes
The Relationship Between Harmful Nonnative Species and Adverse Effects
to Physical Habitat
As discussed at length above, we found harmful nonnative species to
be a significant and widespread factor that continues to drive further
declines in and extirpations of gartersnake populations. Also in our
review of the literature, we found various threats have affected, and
continue to affect, primary components of the physical habitat required
by northern Mexican and narrow-headed gartersnakes. These activities
result in the loss of stream flow, and include examples such as dams,
water diversions, groundwater pumping, and development. Researchers
agree that the period from 1850 to 1940 marked the greatest loss and
degradation of riparian and aquatic communities in Arizona, many of
which were caused by anthropogenic (human-caused) land uses and the
primary and secondary effects of those uses (Stromberg et al. 1996, p.
114; Webb and Leake 2005, pp. 305-310). An estimated one-third of
Arizona's pre-settlement wetlands has dried or been rendered
ecologically dysfunctional (Yuhas 1996, entire). However, not all
aquatic and riparian habitats in the United States that support
northern Mexican or narrow-headed gartersnakes have been significantly
degraded or lost. Despite the loss or modification of aquatic and
riparian habitat we describe below, large reaches of the Verde, Salt,
San Pedro, and Gila Rivers, as well as several of their tributaries,
remain functionally suitable as physical habitat for either gartersnake
species. When we use the term ``physical habitat,'' we refer to the
structural integrity of aquatic and terrestrial components to habitat,
such as plant species richness, density, available water, and any
feature of habitat that does not pertain to the animal community. The
animal community (the prey and predator species that co-occur within
habitat) is not considered in our usage of ``physical habitat,'' for
reasons described immediately below.
Our treatment of how various threats may affect the northern
Mexican or narrow-headed gartersnake is based, in part, on recent
observations made in Mexico that illustrate the relationship of
gartersnakes' physical habitat suitability to the presence of native
prey species and the lack of harmful nonnative species (predators on or
competitors with the northern Mexican gartersnake and narrow-headed
gartersnake), and the presence, or lack thereof, of attributes
associated with these gartersnakes' physical habitat. In 2007, two
groups consisting of agency biologists (including U.S. Fish and
Wildlife Service staff), species experts, and field technicians
conducted numerous gartersnake surveys in Durango and Chihuahua, Mexico
(Burger 2007, p. 1). In the state of Durango, 19 survey sites provided
observation records for 144 gartersnakes, representing five different
species, including the northern Mexican gartersnake (Burger et al.
2010, p. 13). In
[[Page 41524]]
the state of Chihuahua, 12 survey sites provided observation records
for 50 gartersnakes, representing two species, including the northern
Mexican gartersnake (Burger et al. 2010, p. 13). A main reason for this
survey trip was to collect genetic samples from the subspecies
described, at that time, under Thamnophis rufipunctatus, chiefly T. r.
unilabialis and T. r. nigronuchalis. The genetic samples collected
ultimately provided the evidence for the current taxonomic status of
the narrow-headed gartersnake proposed by Wood et al. (2011, entire).
While considerable gartersnake habitat in Mexico is affected by the
presence of harmful nonnative species (Conant 1974, pp. 471, 487-489;
Contreras Balderas and Lozano 1994, pp. 383-384; Unmack and Fagan 2004,
p. 233; Miller et al. 2005, pp. 60-61; Rosen and Melendez 2006, p. 54;
Luja and Rodr[iacute]guez-Estrella 2008, pp. 17-22), Burger (2007, pp.
1-72) surveyed several sites in remote areas that appeared to be free
of nonnative species. In some sites, the physical habitat for northern
Mexican gartersnakes and similar species of gartersnakes appeared to be
in largely good condition, but few or no gartersnakes were detected. At
other sites, the physical habitat was drastically affected by
overgrazing, rural development, or road crossings; however,
gartersnakes were relatively easily detected, which indicated that
population densities were adequate. It should be noted that we do not
have the necessary data to calculate population trends at sampled
localities. Riparian and aquatic habitats in Arizona and New Mexico are
in relatively better physical condition compared to observations of
these habitats made in Durango and Chihuahua, Mexico. However,
nonnative species are also ubiquitous in these same habitats across the
landscape in the southwestern United States, based on our literature
review and GIS modeling. Several sites visited by Burger (2007, pp. 1-
72) in Durango and Chihuahua, Mexico, had physical habitat in poor to
very poor condition, but were largely free of nonnative species. These
situations are rarely encountered in Arizona and New Mexico and,
therefore, provided Burger (2007, pp. 1-72) a unique opportunity to
examine differences in gartersnake population densities based on
condition of the physical habitat, without the confounding effect of
nonnative species on resident gartersnake populations.
Burger (2007, pp. 6, 12, 36, 41, 58, 63) detected moderate to high
densities of gartersnakes at six sites where their physical habitat was
moderately to highly impacted by land uses, but were largely free of
nonnatives. Burger (2007, pp. 18, 26, 32, 61, 64, 66, 67, 69, 72) also
detected either low densities or no gartersnakes at nine sites where
the physical habitat was in moderate to good condition, but where
nonnative species were detected. Eight streams surveyed by Burger
(2007, pp. 15, 22, 46, 49, 51-52, 54, 62) were largely dewatered and
without fish, and had few to no gartersnake observations. One site
presented an anomaly, 19 northern Mexican gartersnakes and two T.
unilabialis were observed at Rio Papigochic at Temosachic, where
crayfish were noted as abundant, but no other nonnatives were detected
(Burger 2007, p. 67). The disproportionate number of northern Mexican
gartersnakes detected, as compared to the more aquatic T. unilabialis,
may be due to differences in habitat preference, or the potential
disproportionate effect of crayfish on T. unilabialis because of their
more aquatic behavior. Similar data were not collected from the
remaining seven sites, which prevents further evaluation of these sites
in these contexts.
Our observations of gartersnake populations in Mexico provide
evidence for the relative importance of native prey species and the
lack of nonnative species in comparison to the physical attributes of
gartersnake habitat. As a result, we have formulated three general
hypotheses: (1) Northern Mexican and narrow-headed gartersnakes may be
more resilient to adverse effects to physical habitat in the absence of
harmful nonnative species, and therefore, more sensitive to adverse
effects to physical habitat in the presence of harmful nonnative
species; (2) the presence of an adequate prey base is important for
persistence of gartersnake populations regardless of whether or not
harmful nonnative species are present; and (3) detections and effects
from harmful nonnative species appear to decrease from north to south
in the Mexican states of Chihuahua and Durango (from the United States-
Mexico International Border), as discussed in Unmack and Fagan (2004,
pp. 233-243).
Based on field data collected by Burger (2007, entire) and on the
above hypotheses, we evaluated the significance of effects to physical
habitat in the context of the presence or absence of nonnative species.
Effects to the physical habitat of gartersnakes can have varying
effects on the gartersnakes themselves depending on the composition of
their biotic community. In the presence of harmful nonnative species,
effects to physical habitat that negatively affect the prey base for
northern Mexican or narrow-headed gartersnakes are believed to be
comparatively more significant than those that do not. As previously
discussed, harmful nonnative species are largely ubiquitous throughout
the range of northern Mexican and narrow-headed gartersnakes and
therefore exacerbate the effects from threats to their physical
habitat.
Altering or Dewatering Aquatic Habitat
Dams and Diversions--The presence of water is critical for northern
Mexican and narrow-headed gartersnakes, as well as their prey base. Of
all the activities that may threaten their physical habitat, none are
more serious than those that reduce flows or dewater habitat, such as
dams, diversions, flood-control projects, and groundwater pumping. Such
activities are widespread in Arizona. For example, municipal water use
in central Arizona increased by 39 percent from 1998 to 2006 (American
Rivers 2006), and at least 35 percent of Arizona's perennial rivers
have been dewatered, assisted by approximately 95 dams that are in
operation in Arizona today (Turner and List 2007, pp. 3, 9). Larger
dams may prevent movement of fish between populations (which affects
prey availability for northern Mexican and narrow-headed gartersnakes)
and dramatically alter the flow regime of streams through the
impoundment of water (Ligon et al. 1995, pp. 184-189). These diversions
also require periodic maintenance and reconstruction, resulting in
potential habitat damages and inputs of sediment into the active
stream.
Flow regimes within stream systems are a primary factor that shape
fish community assemblages. The timing, duration, intensity, and
frequency of flood events has been altered to varying degrees by the
presence of dams, which has an effect on fish communities.
Specifically, Haney et al. (2008, p. 61) suggested that flood pulses
may help to reduce populations of nonnative species and efforts to
increase the baseflows may assist in sustaining native prey species for
northern Mexican and narrow-headed gartersnakes. However, the
investigators in this study also suggest that, because the northern
Mexican gartersnake preys on both fish and frogs, it may be less
affected by reductions in baseflow of streams (Haney et al. 2008, pp.
82, 93). Collier et al. (1996, p. 16) mentions that water development
projects are one of two main causes of the decline of native fish in
the Salt and Gila rivers of Arizona. Unregulated flows with elevated
discharge events favor native species, and regulated flows, absent
significant
[[Page 41525]]
discharge events, favor nonnative species (Probst et al. 2008, p.
1246). Interactions among native fish, nonnative fish, and flow regimes
were observed in the upper reaches of the East Fork of the Gila River.
Prior to the 1983 and 1984 floods in the Gila River system, native fish
occurrence was limited, while nonnative fish were moderately common.
Following the 1983 flood event, adult nonnative predators were
generally absent, and native fish were subsequently collected in
moderate numbers in 1985 (Propst et al. 1986, p. 83). These
relationships are most readily observed in canyon-bound streams, where
shelter sought by nonnative species during large-scale floods is
minimal (Probst et al. 2008, p. 1249). Probst et al. (2008, p. 1246)
also suggested the effect of nonnative fish species on native fish
communities may be most significant during periods of natural drought
(simulated by artificial dewatering).
Effects from flood control projects threaten riparian and aquatic
habitat, as well as threaten the northern Mexican gartersnake directly
in lower Tonto Creek. Kimmell (2008, pers. comm.), Gila County Board of
Supervisors (2008, pers. comm.), Trammell (2008, pers. comm.), and
Sanchez (2008, pers. comm.) all discuss a growing concern of residents
that live within or adjacent to the floodplain of Tonto Creek in Gila
County, Arizona, both upstream and downstream of the town of Gisela,
Arizona. Specifically, there is growing concern to address threats to
private property and associated infrastructure posed by flooding of
Tonto Creek (Sanchez 2008, pers. comm.). An important remaining
population of northern Mexican gartersnakes within the large Salt River
subbasin occurs on Tonto Creek. In Resolution No. 08-06-02, the Gila
County Board of Supervisors proactively declared a state of emergency
within Gila County as a result of the expectation for heavy rain and
snowfall causing repetitive flooding conditions (Gila County Board of
Supervisors 2008, pers. comm.). In response, the Arizona Division of
Emergency Management called meetings and initiated discussions among
stakeholders in an attempt to mitigate these flooding concerns (Kimmell
2008, pers. comm., Trammell 2008, pers. comm.).
Mitigation measures that have been discussed include removal of
riparian vegetation, removal of debris piles, potential channelization
of Tonto Creek, improvements to existing flood control structures or
addition of new structures, and the construction of new bridges.
Adverse effects from these types of activities to aquatic and riparian
habitat, and to the northern Mexican gartersnake or its prey species,
will result from the physical alteration or destruction of habitat,
significant increases to flow velocity, and removal of key foraging
habitat and areas to hibernate, such as debris jams. Specifically,
flood control projects permanently alter stream flow characteristics
and have the potential to make the stream unsuitable as habitat for the
northern Mexican gartersnake by reducing or eliminating stream
sinuosity and associated pool and backwater habitats that are critical
to northern Mexican gartersnakes and their prey species. Threats
presented by these flood control planning efforts are considered
imminent.
Many streams in New Mexico, currently or formerly occupied by
northern Mexican or narrow-headed gartersnakes, have been or could be
affected by water withdrawals. Approximately 9.5 river mi (15.3 km) of
the Gila River mainstem in New Mexico, from Little Creek to the Gila
Bird Area, are in private ownership and have been channelized, and the
water is largely used for agricultural purposes (Hellekson 2012a, pers.
comm.). In addition, the Hooker Dam has been proposed in the reach
above Mogollon Creek and below Turkey Creek as part of the Central
Arizona Project, but remains in deferment status (Hellekson 2012a,
pers. comm.). If constructed, Hooker Dam would significantly alter or
reduce stream flow; favor nonnative, spiny-rayed fish species; and
likely render the affected reach unsuitable for narrow-headed
gartersnakes. Below the Gila Bird Area, but above the Middle Box of the
mainstem Gila River, several water diversions have reduced stream flow
(Hellekson 2012a, pers. comm.). Channelization has also affected a
privately owned reach of Whitewater Creek from the Catwalk downstream
to Glenwood, New Mexico (Hellekson 2012a, pers. comm.). The Gila River
downstream of the town of Cliff, New Mexico, flows through a broad
valley where irrigated agriculture and livestock grazing are the
predominant uses. Human settlement has increased since 1988 (Propst et
al. 2008, pp. 1237-1238). Agricultural practices have led to dewatering
of the river in the Cliff-Gila valley at times during the dry season
(Soles 2003, p. 71). For those portions of the Gila River downstream of
the Arizona-New Mexico border, agricultural diversions and groundwater
pumping have caused declines in the water table, and surface flows in
the central portion of the river basin are diverted for agriculture
(Leopold 1997, pp. 63-64; Tellman et al. 1997, pp. 101-104).
The San Francisco River in New Mexico has undergone sedimentation,
riparian habitat degradation, and extensive water diversion, and at
present has an undependable water supply throughout portions of its
length. The San Francisco River is seasonally dry in the Alma Valley,
and two diversion structures fragment habitat in the upper Alma Valley
and at Pleasanton (NMDGF 2006, p. 302). An approximate 2-stream-mi
(3.2-km) reach of the lower San Francisco River between the Glenwood
Diversion and Alma Bridge, which would otherwise be good narrow-headed
gartersnake habitat, has been completely dewatered by upstream
diversions (Hellekson 2012a, pers. comm.).
Additional withdrawals of water from the Gila and San Francisco
Rivers may occur in the future (McKinnon 2006d). Implementation of
Title II of the Arizona Water Settlements Act (AWSA) (Pub. L. 108-451)
would facilitate the exchange of Central Arizona Project water within
and between southwestern river basins in Arizona and New Mexico, and
may result in the construction of new water development projects.
Section 212 of the AWSA pertains to the New Mexico Unit of the Central
Arizona Project. The AWSA provides for New Mexico water users to
deplete 140,000 acre-feet of additional water from the Gila Basin in
any 10-year period. The settlement also provides the ability to divert
that water without complaint from downstream pre-1968 water rights in
Arizona. New Mexico will receive $66 million to $128 million in non-
reimbursable federal funding. The Interstate Stream Commission (ISC)
funds may be used to cover costs of an actual water supply project,
planning, environmental mitigation, or restoration activities
associated with or necessary for the project, and may be used on one or
more of 21 alternative projects ranging from Gila National Forest San
Francisco River Diversion/Ditch improvements to a regional water supply
project (the Deming Diversion Project). At this time, it is not known
how the funds will be spent, or which potential alternative(s) may be
chosen. While multiple potential project proposals have been accepted
by the New Mexico Office of the State Engineer (NMOSE) (NMOSE 2011a, p.
1), implementation of the AWSA is still in the planning stages on these
streams, and final notice is expected by the end of 2014. Should water
be diverted from the Gila or San Francisco Rivers, flows would be
diminished and direct and indirect losses and degradation of
[[Page 41526]]
habitat for the narrow-headed gartersnake and its prey species would
result.
In addition to affecting the natural behavior of streams and rivers
through changes in timing, intensity, and duration of flood events,
dams create reservoirs that alter resident fish communities. Water
level fluctuation can affect the degree of benefit to harmful nonnative
fish species. Reservoirs that experience limited or slow fluctuations
in water levels are especially beneficial to harmful nonnative species
whereas reservoirs that experience greater fluctuations in water levels
provide less benefit for harmful nonnative species. The timing of
fluctuating water levels contributes to their effect; a precipitous
drop in water levels during harmful nonnative fish reproduction is most
deleterious to their recruitment. A drop in water levels outside of the
reproductive season of harmful nonnative species has less effect on
overall population dynamics.
The cross-sectional profile of any given reservoir also contributes
to its benefit for harmful nonnative fish species. Shallow reservoir
profiles generally provide maximum space and elevated water
temperatures favorable to reproduction of harmful nonnative species,
and deep reservoir profiles with limited shallow areas provide
commensurately less benefit. Examples of reservoirs that benefit
harmful nonnative species, and therefore adversely affect northern
Mexican and narrow-headed gartersnakes (presently or historically),
include Horseshoe and Bartlett Reservoirs on the Verde River, the San
Carlos Reservoir on the Gila River, and Roosevelt, Saguaro, Canyon, and
Apache Lakes on the Salt River. The Salt River Project (SRP) operates
the previously mentioned reservoirs on the Verde and Salt Rivers and,
in the case of Horseshoe and Bartlett Reservoirs, received section
10(a)(1)(B) take authorization under the Act for adverse effects to
several avian and aquatic species (including northern Mexican and
narrow-headed gartersnakes) through a comprehensive threat minimization
and mitigation program found in SRP's habitat conservation plan (SRP
2008, entire). There is no such minimization and mitigation program
developed for the operation Lake Roosevelt, where limited fluctuation
in reservoir levels benefit harmful nonnative species and negatively
affect northern Mexican or narrow-headed gartersnakes and their prey
bases in Tonto Creek and the upper Salt River. A detailed analysis of
the effects of reservoir operations on aquatic communities is provided
in our intra-Service biological and conference opinion provided in
USFWS (2008, pp. 112-131).
The Effect of Population Growth and Development on Water Demands
and Gartersnake Habitat--Arizona's population is expected to double
from 5 million to 10 million people by the year 2030, which will put
increasing pressure on water demands (Overpeck 2008). Arizona increased
its population by 474 percent from 1960 to 2006 (Gammage 2008, p. 15),
and is second only to Nevada as the fastest growing State in terms of
human population (Social Science Data Analysis Network (SSDAR) 2000,
p.1). Over approximately the same time period, population growth rates
in Arizona counties where northern Mexican or narrow-headed gartersnake
habitat exists have varied by county but are no less remarkable, and
all are increasing: Maricopa (463 percent); Pima (318 percent); Santa
Cruz (355 percent); Cochise (214 percent); Yavapai (579 percent); Gila
(199 percent); Graham (238 percent); Apache (228 percent); Navajo (257
percent); Yuma (346 percent); LaPaz (142 percent); and Mohave (2,004
percent) (SSDAR 2000). From 1960 to 2006, the Phoenix metropolitan area
alone grew by 608 percent, and the Tucson metropolitan area grew by 356
percent (Gammage 2008, p. 15). Population growth in Arizona is expected
to be focused along wide swaths of land from the international border
in Nogales, through Tucson, Phoenix, and north into Yavapai County
(called the Sun Corridor ``Megapolitan''), and is predicted to have 8
million people by 2030, an 82.5 percent increase from 2000 (Gammage et
al. 2008, pp. 15, 22-23). If build-out occurs as expected, it could
indirectly affect (through increased recreation pressure and demand for
water) currently occupied habitat for the northern Mexican or narrow-
headed gartersnake, particularly regional populations in Red Rock
Canyon in extreme south-central Arizona, lower Cienega Creek near Vail,
Arizona, and the Verde Valley.
The effect of the increased water withdrawals may be exacerbated by
the current, long-term drought facing the arid southwestern United
States. Philips and Thomas (2005, pp. 1-4) provided stream flow records
that indicate that the drought Arizona experienced between 1999 and
2004 was the worst drought since the early 1940s and possibly earlier.
The Arizona Drought Preparedness Plan Monitoring Technical Committee
(ADPPMTC) (2012) determined the drought status within the Arizona
distributions of northern Mexican and narrow-headed gartersnakes,
through June 2012, to be in ``severe drought.'' Ongoing drought
conditions have depleted recharge of aquifers and decreased base flows
in the region. While drought periods have been relatively numerous in
the arid Southwest from the mid-1800s to the present, the effects of
human-caused impacts on riparian and aquatic communities have
compromised the ability of these communities to function under the
additional stress of prolonged drought conditions. We further discuss
the effect of climate change-induced drought below.
The Arizona Department of Water Resources (ADWR) manages water
supplies in Arizona and has established five Active Management Areas
(AMAs) across the State (ADWR 2006, entire). An AMA is established by
ADWR when an area's water demand has exceeded the groundwater supply
and an overdraft has occurred. In these areas, groundwater use has
exceeded the rate where precipitation can recharge the aquifer.
Geographically, these five AMAs overlap the historical distribution of
the northern Mexican or narrow-headed gartersnake, or both, in Arizona.
The establishment of these AMAs further illustrates the condition of
and future threats to riparian habitat in these areas and are a cause
of concern for the long-term maintenance of northern Mexican and
narrow-headed gartersnake habitat. Such overdrafts reduce surface water
flow of streams that are hydrologically connected to the aquifer, and
these overdrafts can be further exacerbated by surface water
diversions, placing further stress on the aquifer. The presence of
water is a primary habitat component for northern Mexican and narrow-
headed gartersnakes. Existing water laws in Arizona and New Mexico are
inadequate to protect gartersnake habitat from the dewatering effects
of groundwater withdrawals. New Mexico water law does not include
provisions for instream water rights to protect fish and wildlife and
their habitats. Arizona water law does recognize such provisions;
however, because this change is relatively recent, instream water
rights have low priority, and are often never fulfilled because more
senior diversion rights have priority. Gelt (2008, pp. 1-12)
highlighted the fact that existing water laws are outdated and reflect
a legislative interpretation of the resource that is not consistent
with current scientific understanding, such as the important connection
between groundwater and surface water.
Water for development and urbanization is often supplied by
[[Page 41527]]
groundwater pumping and surface water diversions from sources that
include reservoirs and Central Arizona Project's allocations from the
Colorado River. The hydrologic connection between groundwater and
surface flow of intermittent and perennial streams is becoming better
understood. Groundwater pumping creates a cone of depression within the
affected aquifer that slowly radiates outward from the well site. When
the cone of depression intersects the hyporheic zone of a stream (the
active transition zone between two adjacent ecological communities
under or beside a stream channel or floodplain between the surface
water and groundwater that contributes water to the stream itself), the
surface water flow may decrease, and the subsequent drying of riparian
and wetland vegetative communities can follow. Continued groundwater
pumping at such levels draws down the aquifer sufficiently to create a
water-level gradient away from the stream and floodplain (Webb and
Leake 2005, p. 309). Finally, complete disconnection of the aquifer and
the stream results in strong negative effects to riparian vegetation
(Webb and Leake 2005, p. 309). The hyporheic zone can promote ``hot
spots'' of productivity where groundwater upwelling produces nitrates
that can enhance the growth of vegetation, but its significance is
contingent upon its activity and extent of connection with the
groundwater (Boulton et al. 1998, p. 67; Boulton and Hancock 2006, pp.
135, 138). If complete disconnection occurs, the hyporheic zone could
be adversely affected. Such ``hot spots'' can enhance the quality of
northern Mexican and narrow-headed gartersnake habitat. Conversely,
changes to the duration and timing of upwelling can potentially lead to
localized extinctions in biota (Boulton and Hancock 2006, p. 139),
reducing or eliminating gartersnake habitat suitability.
The arid southwestern United States is characterized by limited
annual precipitation, which means limited annual recharge of
groundwater aquifers; even modest changes in groundwater levels from
groundwater pumping can affect above-ground stream flow as evidenced by
depleted flows in the Santa Cruz, Verde, San Pedro, Blue, and lower
Gila rivers as a result of regional groundwater demands (Fernandez and
Rosen 1996, p. 70; Stromberg et al. 1996, pp. 113, 124-128; Rinne et
al. 1998, p. 9; Voeltz 2002, pp. 45-47, 69-71; Haney et al. 2009 p. 1).
Demands are expected to exceed flows in Arivaca Creek, Babocomari
River, lower Cienega Creek, San Pedro River, upper Verde River, and
Agua Fria River (Haney et al. 2009 p. 3, Table 2), which historically
or currently support northern Mexican or narrow-headed gartersnake
populations. The complete loss of surface flow would result in local or
regional extirpations of both species, or limit the species' recovery
in these areas.
Water depletion is a concern for the Verde River (American Rivers
2006; McKinnon 2006a). Barnett and Hawkins (2002, Table 4) reported
population census data from 1970, as well as projections for 2030, for
communities situation along the middle Verde River or within the Verde
River subbasin as a whole, such as Clarkdale, Cottonwood, Jerome, and
Sedona. From 1970-2000, population growth was recorded as Clarkdale
(384 percent), Cottonwood (352 percent), Jerome (113 percent), and
Sedona (504 percent) (Barnett and Hawkins 2002, Table 4). Projected
growth in these same communities from 1970-2030 was tabulated at
Clarkdale (620 percent), Cottonwood (730 percent), Jerome (292
percent), and Sedona (818 percent) (Barnett and Hawkins 2002, Table 4).
These examples of documented and projected population growth within the
Verde River subbasin indicate ever-increasing water demands that have
impacted base flow in the Verde River and are expected to continue. The
middle and lower Verde River has limited or no flow during portions of
the year due to agricultural diversion and upstream impoundments, and
has several impoundments in its middle reaches, which could expand the
area of impacted northern Mexican and narrow-headed gartersnake
habitat. Blasch et al. (2006, p. 2) suggests that groundwater storage
in the Verde River subbasin has already declined due to groundwater
pumping and reductions in natural channel recharge resulting from
stream flow diversions.
Also impacting water in the Verde River, the City of Prescott,
Arizona, experienced a 22 percent increase in population between 2000
and 2005 (U.S. Census Bureau 2010, p. 1), averaging around 4 percent
growth per year (City of Prescott 2010, p. 1). In addition, the towns
of Prescott Valley and Chino Valley experienced growth rates of 66 and
67 percent, respectively (Arizona Department of Commerce 2009a, p. 1;
2009b, p. 1). This growth is facilitated by groundwater pumping in the
Verde River basin. In 2004, the cities of Prescott and Prescott Valley
purchased a ranch in the Big Chino basin in the headwaters of the Verde
River, with the intent of drilling new wells to supply up to
approximately 4,933,927 cubic meters (4,000 acre-feet (AF)) of
groundwater per year. If such drilling occurs, it could have serious
adverse effects on the mainstem and tributaries of the Verde River.
Scientific studies have shown a link between the Big Chino aquifer
and spring flows that form the headwaters of the Verde River. It is
estimated that 80 to 86 percent of baseflow in the upper Verde River
comes from the Big Chino aquifer (Wirt 2005, p. G8). However, while
these withdrawals could potentially dewater the upper 26 mi (42 km) of
the Verde River (Wirt and Hjalmarson 2000, p. 4; Marder 2009, pp. 188-
189), it is uncertain that this project will occur given the legal and
administrative challenges it faces; however, an agreement in principle
was signed between various factions associated with water rights and
interests on the Verde River (Citizens Water Advocacy Group 2010; Verde
Independent 2010, p. 1). An indepth discussion of the effects to Verde
River from pumping of the Big Chino Aquifer is available in Marder
(2009, pp. 183-189). Within the Verde River subbasin, and particularly
within the Verde Valley, where the northern Mexican and narrow-headed
gartersnakes could occur, several other activities continue to threaten
surface flows (Rinne et al. 1998, p. 9; Paradzick et al. 2006, pp. 104-
110). Many tributaries of the Verde River are permanently or seasonally
dewatered by water diversions for agriculture (Paradzick et al. 2006,
pp. 104-110). The demands for surface water allocations from rapidly
growing communities and agricultural and mining interests have altered
flows or dewatered significant reaches during the spring and summer
months in some of the Verde River's larger, formerly perennial
tributaries such as Wet Beaver Creek, West Clear Creek, and the East
Verde River (Girmendonk and Young 1993, pp. 45-47; Sullivan and
Richardson 1993, pp. 38-39; Paradzick et al. 2006, pp. 104-110), which
may have supported either the northern Mexican or narrow-headed
gartersnake, or both. Groundwater pumping in the Tonto Creek drainage
regularly eliminates surface flows during parts of the year (Abarca and
Weedman 1993, p. 2).
Further south in Arizona, portions of the San Pedro River are now
classified as formerly perennial (The Nature Conservancy 2006), and
water withdrawals are a concern for the San Pedro River. The Cananea
Mine in Sonora, Mexico, owns the land surrounding the headwaters of the
San Pedro. There is disagreement on the
[[Page 41528]]
exact amount of water withdrawn by the mine, Mexicana de Cananea, which
is one of the largest open-pit copper mines in the world. However,
there is agreement that it is the largest water user in the basin
(Harris et al. 2001; Varady et al. 2000, p. 232). Along the upper San
Pedro River, Stromberg et al. (1996, pp. 124-127) found that wetland
herbaceous species, important as cover for northern Mexican
gartersnakes, are the most sensitive to the effects of a declining
groundwater level. Webb and Leake (2005, pp. 302, 318-320) described a
correlative trend regarding vegetation along southwestern streams from
historically being dominated by marshy grasslands preferable to
northern Mexican gartersnakes, to currently being dominated by woody
species that are more tolerant of declining water tables due to their
deeper rooting depths.
Another primary groundwater user in the San Pedro subbasin is Fort
Huachuca. Fort Huachuca is a U.S. Army installation located near Sierra
Vista, Arizona. Initially established in 1877 as a camp for the
military, the water rights of the Fort are predated only by those of
local Indian tribes (Varady et al. 2000, p. 230). Fort Huachuca has
pursued a rigorous water use reduction plan, working over the past
decade to reduce groundwater consumption in the Sierra Vista subbasin.
Their efforts have focused primarily on reductions in groundwater
demand both on-post and off-post and increased artificial and enhanced
recharge of the groundwater system. Annual pumping from Fort Huachuca
production wells has decreased from a high of approximately 3,200 acre-
feet (AF) in 1989, to a low of approximately 1,400 AF in 2005. In
addition, Fort Huachuca and the City of Sierra Vista have increased the
amount of water recharged to the regional aquifer through construction
of effluent recharge facilities and detention basins that not only
increase stormwater recharge, but mitigate the negative effects of
increased runoff from urbanization. The amount of effluent that was
recharged by Fort Huachuca and the City of Sierra Vista in 2005 was 426
AF and 1,868 AF, respectively. During this same year, enhanced
stormwater recharge at detention basins was estimated to be 129 AF. The
total net effect of all the combined efforts initiated by Fort Huachuca
has been to reduce the net groundwater consumption by approximately
2,272 AF (71 percent) since 1989 (USFWS 2007, pp. 41-42).
Groundwater withdrawal in Eagle Creek, primarily for water
supplying the large open-pit copper mine at Morenci, Arizona, dries
portions of the stream (Sublette et al. 1990, p. 19; USFWS 2005; Propst
et al. 1986, p. 7) that otherwise supports habitat for narrow-headed
gartersnakes. Mining is the largest industrial water user in
southeastern Arizona. The Morenci mine on Eagle Creek is North
America's largest producer of copper, covering approximately 24,281
hectares (ha) (60,000 acres (ac)). Water for the mine is imported from
the Black River, diverted from Eagle Creek as surface flows, or
withdrawn from the Upper Eagle Creek Well Field (Arizona Department of
Water Resources 2009, p. 1).
The Rosemont Copper Mine proposed to be constructed in the north-
eastern area of the Santa Rita Mountains in Santa Cruz County, Arizona,
will include a mine pit that will be excavated to a depth greater than
that of the regional aquifer. Water will thus drain from storage in the
aquifer into the pit. The need to dewater the pit during mining
operations will thus result in ongoing removal of aquifer water
storage. Upon cessation of mining, a pit lake will form, and
evaporation from this water body will continue to remove water from
storage in the regional aquifer. This aquifer also supplies baseflow to
Cienega Creek, immediately east of the proposed project site. Several
groundwater models have been developed to analyze potential effects of
expected groundwater withdrawals. However, the latest independent
models did not indicate that significant effects to baseflows in
Cienega Creek are expected from the Rosemont Copper Mine into the
foreseeable future.
The best available scientific and commercial information indicates
that, regardless of the scenario, any reduction in the presence or
availability of water is a significant threat to northern Mexican and
narrow-headed gartersnakes, their prey base, and their habitat. This is
because water is a fundamental need that supports the necessary aquatic
and riparian habitats and prey species needed by both species of
gartersnake. Through GIS analyses, we found that approximately 32
percent of formerly perennial streams have been dewatered within the
historical distribution of the northern Mexican gartersnake. Within the
historical distribution of the narrow-headed gartersnake, approximately
13 percent of formerly perennial streams have been dewatered.
Climate Change and Drought--Our analyses under the Act include
consideration of ongoing and projected changes in climate. The terms
``climate'' and ``climate change'' are defined by the Intergovernmental
Panel on Climate Change (IPCC). ``Climate'' refers to the mean and
variability of different types of weather conditions over time, with 30
years being a typical period for such measurements, although shorter or
longer periods also may be used (IPCC 2007, p. 78). The term ``climate
change'' thus refers to a change in the mean or variability of one or
more measures of climate (e.g., temperature or precipitation) that
persists for an extended period, typically decades or longer, whether
the change is due to natural variability, human activity, or both (IPCC
2007, p. 78). Various types of changes in climate can have direct or
indirect effects on species. These effects may be positive, neutral, or
negative and they may change over time, depending on the species and
other relevant considerations, such as the effects of interactions of
climate with other variables (e.g., habitat fragmentation) (IPCC 2007,
pp. 8-14, 18-19). In our analyses, we use our expert judgment to weigh
relevant information, including uncertainty, in our consideration of
various aspects of climate change and their predicted effects on
northern Mexican and narrow-headed gartersnakes.
The ecology and natural histories of northern Mexican and narrow-
headed gartersnakes are strongly linked to water. As discussed above,
the northern Mexican gartersnake is a highly aquatic species and relies
largely upon other aquatic species, such as ranid frogs and native and
nonnative, soft-rayed fish as prey. The narrow-headed gartersnake is
the most aquatic of the southwestern gartersnakes and is a specialized
predator on native and nonnative, soft-rayed fish found primarily in
clear, rocky, higher elevation streams. Because of their aquatic
nature, Wood et al. (2011, p. 3) predict they may be uniquely
susceptible to environmental change, especially factors associated with
climate change. Together, these factors are likely to make northern
Mexican and narrow-headed gartersnakes vulnerable to effects of climate
change and drought discussed below.
Several climate-related trends have been detected since the 1970s
in the southwestern United States including increases in surface
temperatures, rainfall intensity, drought, heat waves, extreme high
temperatures, average low temperatures (Overpeck 2008, entire). Annual
precipitation amounts in the southwestern United States may decrease by
10 percent by the year 2100 (Overpeck 2008, entire). Seager et al.
(2007, pp. 1181-1184) analyzed 19
[[Page 41529]]
different computer models of differing variables to estimate the future
climatology of the southwestern United States and northern Mexico in
response to predictions of changing climatic patterns. All but 1 of the
19 models predicted a drying trend within the Southwest; one predicted
a trend toward a wetter climate (Seager et al. 2007, p. 1181). A total
of 49 projections were created using the 19 models, and all but 3
predicted a shift to increasing aridity (dryness) in the Southwest as
early as 2021-2040 (Seager et al. 2007, p. 1181). Northern Mexican and
particularly narrow-headed gartersnakes, and their prey bases, depend
on permanent or nearly permanent water for survival. A large percentage
of habitats within the current distribution of northern Mexican and
narrow-headed gartersnakes are predicted to be at risk of becoming more
arid with reductions in snow pack levels (Seager et al. 2007, pp. 1183-
1184). This has severe implications for the integrity of aquatic and
riparian ecosystems and the water that supports them. In assessing
potential effects of predicted climate change to river systems in New
Mexico, Molles (2007) found that: (1) Variation in stream flow will
likely be higher than variation in precipitation; (2) predicted effects
such as warming and drying are expected to result in higher variability
in stream flows; and (3) high-elevation fish and non-flying
invertebrates (which are prey for gartersnake prey species) are at
greatest risk from effects of predicted climate change. Enquist and
Gori (2008, p. iii) found that most of New Mexico's mid- to high-
elevation forests and woodlands have experienced either consistently
warmer and drier conditions or greater variability in temperature and
precipitation from 1991 to 2005. However, Enquist et al. (2008, p. v)
found the upper Gila and San Francisco subbasins, which support narrow-
headed gartersnake populations, have experienced very little change in
moisture stress during the same period.
Cavazos and Arriaga (2010, entire) found that average temperatures
along the Mexican Plateau in Mexico could rise by as much as
1.8[emsp14][deg]F (1 [deg]C) in the next 20 years and by as much as
9[emsp14][deg]F (5 [deg]C) in the next 20 years, according to their
models. Cavazos and Arriaga (2010, entire) also found that
precipitation may decrease up to 12 percent over the next 20 years in
the same region, with pronounced decreases in winter and spring
precipitation.
Potential drought associated with changing climatic patterns may
adversely affect the amphibian prey base for the northern Mexican
gartersnake. Amphibians may be among the first vertebrates to exhibit
broad-scale changes in response to changes in global climatic patters
due to their sensitivity to changes in moisture and temperature (Reaser
and Blaustein 2005, p. 61). Changes in temperature and moisture,
combined with the ongoing threat to amphibians from the persistence of
disease causing bacteria such as Batrachochytrium dendrobatidis (Bd)
may cause prey species to experience increased physiological stress and
decreased immune system function, possibly leading to disease outbreaks
(Carey and Alexander 2003, pp. 111-121; Pounds et al. 2006, pp. 161-
167). Of the 30 different vertebrate species in the Sky Island region
of southeastern Arizona, the northern Mexican gartersnake was found to
be the fifth-most vulnerable (total combined score) to predicted
climate change; one of its primary prey species, the Chiricahua leopard
frog, was determined to be the fourth most vulnerable (Coe et al. 2012,
p. 16). Both the northern Mexican gartersnake and the Chiricahua
leopard frog ranked the highest of all species assessed for
vulnerability of their habitat to predicted climate change, and the
Chiricahua leopard frog was also found to be the most vulnerable in
terms of its physiology (Coe et al. 2012, p. 18). Relative uncertainty
for the vulnerability assessment provided by Coe et al. (2012, Table
2.2) ranged from 0 to 8 (higher score means greater uncertainty), and
the northern Mexican gartersnake score was 3, meaning that the
vulnerability assessment was more certain than not. Coe et al. (2012,
entire) focused their assessment of species vulnerability to climate
change on those occurring on the Coronado National Forest in
southeastern Arizona. However, it is not unreasonable to hypothesize
that results might be applicable in a larger, regional context as
applied in most climate models.
The bullfrog, also assessed by Coe et al. (2012, pp. 16, 18, Table
2.2), was shown to be significantly less vulnerable to predicted
climate change than either northern Mexican gartersnakes or Chiricahua
leopard frogs with an uncertainty score of 1 (very certain). We suspect
bullfrogs were found to be less vulnerable by Coe et al. (2012) to
predicted climate change in southeastern Arizona due to their dispersal
and colonization capabilities, capacity for self-sustaining
cannibalistic populations, and ecological dominance where they occur.
Based upon climate change models, nonnative species biology, and
ecological observations, Rahel et al. (2008, p. 551) concluded that
climate change could foster the expansion of nonnative aquatic species
into new areas, magnify the effects of existing aquatic nonnative
species where they currently occur, increase nonnative predation rates,
and heighten the virulence of disease outbreaks in North America.
Rahel and Olden (2008, p. 526) expect that increases in water
temperatures in drier climates such as the southwestern United States
will result in periods of prolonged low flows and stream drying. These
effects from changing climatic conditions may have profound effects on
the amount, permanency, and quality of habitat for northern Mexican and
narrow-headed gartersnakes as well as their prey base. Changes in
amount or type of winter precipitation may affect snowpack levels as
well as the timing of their discharge into high-elevation streams. Low
or no snowpack levels would jeopardize the amount and reliability of
stream flow during the arid spring and early summer months, which would
increase water temperatures to unsuitable levels or eliminate flow
altogether. Harmful nonnative species such as largemouth bass are
expected to benefit from prolonged periods of low flow (Rahel and Olden
2008, p. 527). These nonnative predatory species evolved in river
systems with hydrographs that were largely stable, not punctuated by
flood pulses in which native species evolved and benefit from. Probst
et al. (2008, p. 1246) also suggested that nonnative fish species may
benefit from drought.
Changes to climatic patterns may warm water temperatures, alter
stream flow events, and increase demand for water storage and
conveyance systems (Rahel and Olden 2008, pp. 521-522). Warmer water
temperatures across temperate regions are predicted to expand the
distribution of existing harmful nonnative species, which evolved in
warmer water temperatures, by providing 31 percent more suitable
habitat. This conclusion is based upon studies that compared the
thermal tolerances of 57 fish species with predictions made from
climate change temperature models (Mohseni et al. 2003, p. 389). Eaton
and Scheller (1996, p. 1,111) reported that while several cold-water
fish species (such as trout, a prey species for narrow-headed
gartersnakes) in North America are expected to have reductions in their
distribution from effects of climate change, several harmful nonnative
species are expected to increase their distribution. In the
southwestern United States, this situation may occur where the quantity
of water is sufficient to
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sustain effects of potential prolonged drought conditions but where
water temperature may warm to a level found suitable to harmful
nonnative species that were previously physiologically precluded from
occupation of these areas. Species that are particularly harmful to
northern Mexican and narrow-headed gartersnake populations such as the
green sunfish, channel catfish, largemouth bass, and bluegill are
expected to increase their distribution by 7.4 percent, 25.2 percent,
30.4 percent, and 33.3 percent, respectively (Eaton and Scheller 1996,
p. 1,111).
Vanishing Cienegas--Cienegas are particularly important habitat for
the northern Mexican gartersnake and are considered ideal for the
species because these areas present ideal habitat characteristics for
the species and its prey base and have been shown to support robust
populations of both (Rosen and Schwalbe 1988, p. 14). Hendrickson and
Minckley (1984, p. 131) defined cienegas as ``mid-elevation (3,281-
6,562 ft (1,000-2000 m)) wetlands characterized by permanently
saturated, highly organic, reducing [lowering of oxygen level] soils.''
Many of these unique communities of the southwestern United States,
Arizona in particular, and Mexico have been lost in the past century to
streambed modification, intensive livestock grazing, woodcutting,
artificial drainage structures, stream flow stabilization by upstream
dams, channelization, and stream flow reduction from groundwater
pumping and water diversions (Hendrickson and Minckley 1984, p. 161).
Stromberg et al. (1996, p. 114) state that cienegas were formerly
extensive along streams of the Southwest; however, most were destroyed
during the late 1800s, when groundwater tables declined several meters
and stream channels became incised.
Many sub-basins, where cienegas have been severely modified or lost
entirely, wholly or partially overlap the historical distribution of
the northern Mexican gartersnake, including the San Simon, Sulphur
Springs, San Pedro, and Santa Cruz valleys of southeastern and south-
central Arizona. The San Simon Valley in Arizona possessed several
natural cienegas with abundant vegetation prior to 1885, and was used
as a watering stop for pioneers, military, and surveying expeditions
(Hendrickson and Minckley 1984, pp. 139-140). In the subsequent
decades, the disappearance of grasses and commencement of severe
erosion were the result of historical grazing pressure by large herds
of cattle, as well as the effects from wagon trails that paralleled
arroyos, occasionally crossed them, and often required stream bank
modification (Hendrickson and Minckley 1984, p. 140). Today, only the
artificially maintained San Simon Cienega exists in this valley.
Similar accounts of past conditions, adverse effects from historical
anthropogenic activities, and subsequent reduction in the extent and
quality of cienega habitats in the remaining valleys are also provided
in Hendrickson and Minckley (1984, pp. 138-160).
Development and Recreation within Riparian Corridors--Development
within and adjacent to riparian areas has proven to be a significant
threat to riparian biological communities and their suitability for
native species (Medina 1990, p. 351). Riparian communities are
sensitive to even low levels (less than 10 percent) of urban
development within a subbasin (Wheeler et al. 2005, p. 142).
Development along or within proximity to riparian zones can alter the
nature of stream flow dramatically, changing once-perennial streams
into ephemeral streams, which has direct consequences on the riparian
community (Medina 1990, pp. 358-359). Medina (1990, pp. 358-359)
correlated tree density and age class representation to stream flow,
finding that decreased flow reduced tree densities and generally
resulted in few to no small-diameter trees. Small- diameter trees
assist northern Mexican and narrow-headed gartersnakes by providing
additional habitat complexity, thermoregulatory opportunities, and
cover needed to reduce predation risk and enhance the usefulness of
areas for maintaining optimal body temperature. The presence of small
shrubs and trees may be particularly important for the narrow-headed
gartersnake (Deganhardt et al. 1996, p. 327). Development within
occupied riparian habitat also likely increases the number of human-
gartersnake encounters and therefore the frequency of adverse human
interaction, described below.
Obvious examples of the influence of urbanization and development
can be observed within the areas of greater Tucson and Phoenix,
Arizona, where impacts have modified riparian vegetation, structurally
altered stream channels, facilitated nonnative species introductions,
and dewatered large reaches of formerly perennial rivers where the
northern Mexican gartersnake historically occurred (Santa Cruz, lower
Gila, and lower Salt Rivers, respectively). Urbanization and
development of these areas, along with the introduction of nonnative
species, are largely responsible for the likely extirpation of the
northern Mexican gartersnake from these regions.
Development near riparian areas usually leads to increased
recreation. Riparian areas located near urban areas are vulnerable to
the effects of increased recreation. An example of such an area within
the existing distribution of both the northern Mexican and narrow-
headed gartersnake is the Verde Valley. The reach of the Verde River
that winds through the Verde Valley receives a high amount of
recreational use from people living in central Arizona (Paradzick et
al. 2006, pp. 107-108). Increased human use results in the trampling of
near-shore vegetation, which reduces cover for gartersnakes, especially
newborns. Increased human visitation in occupied habitat also increases
the potential for adverse human interactions with gartersnakes, which
frequently leads to the capture, injury, or death of the snake (Rosen
and Schwalbe 1988, p. 43; Ernst and Zug 1996, p. 75; Green 1997, pp.
285-286; Nowak and Santana-Bendix 2002, pp. 37-39).
Oak Creek Canyon, which represents an important source population
for narrow-headed gartersnakes, is also a well-known example of an area
with very high recreation levels. Recreational activities in the
Southwest are often heavily tied to water bodies and riparian areas,
due to the general lack of surface water on the landscape. Increased
recreational impacts on the quantity and quality of water, as well as
the adjacent vegetation, negatively affect northern Mexican and narrow-
headed gartersnakes. The impacts to riparian habitat from recreation
can include movement of people or livestock, such as horses or mules,
along stream banks, trampling, loss of vegetation, and increased danger
of fire starts (Northern Arizona University 2005, p. 136; Monz et al.
2010, pp. 553-554). In the arid Gila River Basin, recreational impacts
are disproportionately distributed along streams as a primary focus for
recreation (Briggs 1996, p. 36). Within the range of the northern
Mexican and narrow-headed gartersnakes in the United States, the
majority of the occupied areas occur on Federal lands, which are
managed for recreation and other purposes. On the Gila National Forest,
heavy recreation use within occupied narrow-headed gartersnake habitat
is thought to impact populations along the Middle Fork Gila River, the
mainstem Gila River between Cliff Dwellings and Little Creek, and
Whitewater Creek from the Catwalk to Glenwood (Hellekson 2012a, pers.
comm.).
Urbanization on smaller scales can also impact habitat suitability
and the prey base for the northern Mexican or
[[Page 41531]]
narrow-headed gartersnakes, such as along Tonto Creek, within the Verde
Valley, and the vicinity of Rock Springs along the Agua Fria River
(Girmendonk and Young 1997, pp. 45-52; Voeltz 2002, pp. 58-59, 69-71;
Holycross et al.2006, pp. 53, 56; Paradzick et al. 2006, pp. 89-90).
One of the most stable populations of the northern Mexican gartersnake
in the United States, at the Page Springs and Bubbling Ponds fish
hatcheries along Oak Creek, is threatened by ongoing small-scale
development projects that may adversely affect the northern Mexican
gartersnake directly through physical harm or injury or indirectly from
effects to its habitat or prey base (AGFD 1997a, p. 8; AGFD 1997b, p.
4). Current and future management and maintenance of Bubbling Ponds
include a variety of activities that would potentially affect snake
habitat, such as the maintenance of roads, buildings, fences, and
equipment, as well as development (residences, storage facilities,
asphalt, resurfacing, etc.) and both human- and habitat-based
enhancement projects (AGFD 1997b, pp. 8-9; Wilson and Company 1991, pp.
1-40; 1992, pp. 1-99). However, we expect adaptive management in
relation to activities at the hatcheries, as informed by population
studies that have occurred there, will help reduce the overall effects
to this critical northern Mexican gartersnake population and avoid
extirpation of this important population.
Diminishing Water Quantity and Quality in Mexico--While effects to
riparian and aquatic communities affect both the northern Mexican
gartersnake and the narrow-headed gartersnake in the United States,
Mexico provides habitat only for the northern Mexican gartersnake.
Threats to northern Mexican gartersnake habitat in Mexico include
intensive livestock grazing, urbanization and development, water
diversions and groundwater pumping, loss of vegetation cover and
deforestation, and erosion, as well as impoundments and dams that have
modified or destroyed riparian and aquatic communities in areas of
Mexico where the species occurred historically. Rorabaugh (2008, pp.
25-26) noted threats to northern Mexican gartersnakes and their native
amphibian prey base in Sonora, which included disease, pollution,
intensive livestock grazing, conversion of land for agriculture,
nonnative plant invasions, and logging. Ramirez Bautista and Arizmendi
(2004, p. 3) stated that the principal threats to northern Mexican
gartersnake habitat in Mexico include the drying of wetlands, intensive
livestock grazing, deforestation, wildfires, and urbanization. In
addition, nonnative species, such as bullfrogs and nonnative, spiny-
rayed fish, have been introduced throughout Mexico and continue to
disperse naturally, broadening their distributions (Conant 1974, pp.
487-489; Miller et al. 2005, pp. 60-61; Luja and Rodr[iacute]guez-
Estrella 2008, pp. 17-22).
Mexico's water needs for urban and agricultural development, as
well impacts to aquatic habitat from these uses, are linked to
significant human population growth over the past century in Mexico.
Mexico's human population grew 700 percent from 1910 to 2000 (Miller et
al. 2005, p. 60). Mexico's population increased by 245 percent from
1950 to 2002, and is projected to grow by another 28 percent by 2025
(EarthTrends 2005). Growth is concentrated in Mexico's northern states
(Stoleson et al. 2005, Table 3.1) and is now skewed towards urban areas
(Miller et al. 2005, p. 60). The human population of Sonora, Mexico,
doubled in size from 1970 (1.1 million) to 2000 (2.2 million) (Stoleson
et al. 2005, p. 54). The population of Sonora is expected to increase
by 23 percent, to 2.7 million people, in 2020 (Stoleson et al. 2005, p.
54). Increasing trends in Mexico's human population will continue to
place additional stress on the country's freshwater resources and
continue to be the catalyst for the elimination of northern Mexican
gartersnake habitat and prey species.
Much knowledge of the status of aquatic ecosystems in Mexico has
come from fisheries research, which is particularly applicable to
assessing the status of northern Mexican gartersnakes because of the
gartersnakes' dependency on a functioning prey base. Fisheries research
is also particularly applicable because of the role fishes serve as
indicators of the status of the aquatic community as a whole. Miller et
al. (2005) reported information on threats to freshwater fishes, and
riparian and aquatic communities in specific water bodies from several
regions throughout Mexico within the range of the northern Mexican
gartersnake: the R[iacute]o Grande (dam construction, p. 78 and
extirpations of freshwater fish species, pp. 82, 112); headwaters of
the R[iacute]o Lerma (extirpation of freshwater fish species, nonnative
species, pollution, dewatering, pp. 60, 105, 197); Lago de Chapala and
its outlet to the R[iacute]o Grande de Santiago (major declines in
freshwater fish species, p. 106); medium-sized streams throughout the
Sierra Madre Occidental (localized extirpations, logging, dewatering,
pp. 109, 177, 247); the R[iacute]o Conchos (extirpations of freshwater
fish species, p. 112); the r[iacute]os Casas Grandes, Santa
Mar[iacute]a, del Carmen, and Laguna Bustillos (water diversions,
groundwater pumping, channelization, flood control practices,
pollution, and introduction of nonnative species, pp. 124, 197); the
R[iacute]o Santa Cruz (extirpations, p. 140); the R[iacute]o Yaqui
(nonnative species, pp. 148, Plate 61); the R[iacute]o Colorado
(nonnative species, p. 153); the r[iacute]os Fuerte and Culiac[aacute]n
(logging, p. 177); canals, ponds, lakes in the Valle de M[eacute]xico
(nonnative species, extirpations, pollution, pp. 197, 281); the
R[iacute]o Verde Basin (dewatering, nonnative species, extirpations,
Plate 88); the R[iacute]o Mayo (dewatering, nonnative species, p. 247);
the R[iacute]o Papaloapan (pollution, p. 252); lagos de Zacapu and
Yuriria (habitat destruction, p. 282); and the R[iacute]o P[aacute]nuco
Basin (nonnative species, p. 295).
Excessive sedimentation also appears to be a significant problem
for aquatic habitat in Mexico. Recent estimates indicate that 80
percent of Mexico is affected by soil erosion caused by vegetation
removal related to grazing, fires, agriculture, deforestation, etc. The
most serious erosion is occurring in the states of Guanajuato (43
percent of the state's land area), Jalisco (25 percent of the state's
land area), and M[eacute]xico (25 percent of the state's land area) (va
Landa et al. 1997, p. 317), all of which occur within the distribution
of the northern Mexican gartersnake. Miller et al. (2005, p. 60) stated
that ``During the time we have collectively studied fishes in
M[eacute]xico and southwestern United States, the entire biotas of long
reaches of major streams such as the R[iacute]o Grande de Santiago
below Guadalajara (Jalisco) and R[iacute]o Colorado (lower Colorado
River in Mexico) downstream of Hoover (Boulder) Dam (in the United
States), have simply been destroyed by pollution and river
alteration.'' These streams are within the distribution of the northern
Mexican gartersnake. The geographic extent of threats reported by
Miller et al. (2005) across the distribution of the northern Mexican
gartersnake in Mexico is evidence that they are widespread through the
country, and encompass a large proportion of the distribution of the
northern Mexican gartersnake in Mexico.
In northern Mexico, effects of development, such as agriculture and
irrigation practices on streams and rivers in Sonora have been
documented at least as far back as the 1960s. Branson et al. (1960, p.
218) found that the perennial rivers that drain the Sierra Madre are
``silt-laden and extremely turbid, mainly because of irrigation
practices.'' Smaller mountain streams,
[[Page 41532]]
such as the Rio Nacozari in Sonora were found to be ``biological
deserts'' from the effects of numerous local mining practices (Branson
et al. 1960, p. 218). These perennial rivers and their mountain
tributaries were historically occupied by northern Mexican gartersnakes
and their prey species whose populations have since been adversely
affected and may be extirpated.
Minckley et al. (2002, pp. 687-705) provided a summary of threats
(p. 696) to three newly described (at the time) species of pupfish and
their habitat in Chihuahua, Mexico, within the distribution of the
northern Mexican gartersnake. Initial settlement and agricultural
development of the area resulted in significant channel cutting through
soil layers protecting the alluvial plain above them, which resulted in
reductions in the base level of each basin in succession (Minckley et
al. 2002, pp. 696). Related to these activities, the building of dams
and diversion structures dried entire reaches of some regional streams
and altered flow patterns of others (Minckley et al. 2002, pp. 696).
This was followed by groundwater pumping (enhanced by the invention of
the electric pump), which lowered groundwater levels and dried up
springs and small channels and reduced the reliability of baseflow in
``essentially all systems'' (Minckley et al. 2002, pp. 696).
Subsequently, the introduction and expansion of nonnative species in
the area successfully displaced or extirpated many native species
(Minckley et al. 2002, pp. 696). Conant (1974, pp. 486-489) described
significant threats to northern Mexican gartersnake habitat within its
distribution in western Chihuahua, Mexico, and within the Rio Concho
system where it occurs. These threats included impoundments, water
diversions, and purposeful introductions of largemouth bass, common
carp, and bullfrogs.
In the central portions of the northern Mexican gartersnakes' range
in Mexico, such as in Durango, Mexico, population growth since the
1960s has led to regional effects such as reduced stream flow,
increased water pollution, and largemouth bass introductions, which
``have seriously affected native biota'' (Miller et al. 1989, p. 26).
McCranie and Wilson (1987, p. 2) discuss threats to the pine-oak
communities of higher elevation habitats within the distribution of the
northern Mexican gartersnake in the Sierra Madre Occidental in Mexico,
specifically noting that `` . . . the relative pristine character of
the pine-oak woodlands is threatened . . . every time a new road is
bulldozed up the slopes in search of new madera or pasturage. Once the
road is built, further development follows; pueblos begin to pop up
along its length. . . .'' Several drainages that possess suitable
habitat for the northern Mexican gartersnake occur in the area
referenced above by McCranie and Wilson (1987, p. 2) including the Rio
de la Cuidad, Rio Quebrada El Salto, Rio Chico, Rio Las Bayas, Rio El
Cigarrero, Rio Galindo, Rio Santa Barbara, and the Rio Chavaria.
In the southern portion of the northern Mexican gartersnakes' range
in Mexico, growth and development around Mexico City resulted in
agricultural practices and groundwater demands that dewatered aquatic
habitat and led to declines, and in some cases, extinctions of local
native fish species (Miller et al. 1989, p. 25). In the region of
southern Coahuila, Mexico, habitat modification and the loss of
springs, water pollution, and irrigation practices has adversely
affected native fish populations and led to the extinction of several
native fish species (Miller et al. 1989, pp. 28-33). Considerable
research has been focused in the central and west-central regions of
Mexico, within the southern portion of the northern Mexican
gartersnake's range, where native fish endemism (unique, narrowly
distributed Suite of species) is high, as are threats to their
populations and habitat. Since the 1970s in central Mexico, significant
human population growth has resulted in the overexploitation of local
fisheries and water pollution; these factors have accelerated the
degradation of stream and riverine habitats and led to fish communities
becoming reduced or undergoing significant changes in structure and
composition (Mercado-Silva et al. 2002, p. 180). These shifts in fish
community composition, population density, and shrinking distributions
have adversely affected the northern Mexican gartersnake prey base in
the southern portion of its range in Mexico. The Lerma River basin is
the largest in west-central Mexico and is within the distribution of
the northern Mexican gartersnake in the states of Jalisco, Guanajuato,
and Quer[eacute]taro in the southern portion of its range. Lyons et al.
(1995, p. 572) reported that many fish communities in large perennial
rivers, isolated spring-fed streams, or spring sources themselves of
this region have been ``radically restructured'' and are now dominated
by a few nonnative, generalist species. Lowland streams and rivers in
this region are used heavily for irrigation and are polluted by
industrial, municipal, and agricultural discharges (Lyons and Navarro-
Perez 1990, p. 37; Lyons et al. 1995, p. 572).
Native fish communities of west-central Mexico have been found to
be in serious decline as a result of habitat degradation at an
``unprecedented'' rate due to water withdrawals (diversions for
irrigation), as well as untreated municipal, industrial, and
agricultural discharges (Lyons et al. 1998, pp. 10-11). Numerous dams
have been built along the Lerma River and along its major tributaries
to support one of Mexico's most densely populated regions during the
annual dry period; the water is used for irrigation, industry, and
human consumption (Lyons et al. 1998, p. 11). From 1985 to 1993, Lyons
et al. (1998, p. 12) found that 29 of 116 (25 percent) fish sampling
locations visited within the Lerma River watershed were completely dry
and another 30 were too polluted to support a fish community. These
figures indicate that over half of the localities visited by Lyons et
al. (1998, p. 12) that maintained fish populations prior to 1985 no
longer support fish, which has likely led to local northern Mexican
gartersnake population declines or extirpations. Soto-Galera et al.
(1999, p. 137) reported fish and water quality sampling results from 20
locations within the Rio Grande de Morelia-Lago de Cuitzeo Basin of
Michoac[aacute]n and Guanajuato, Mexico, and found that over the past
several decades, diminishing water quantity and worsening water quality
have resulted in the elimination of 26 percent of native fish species
from the basin, the extinction of two species of native fish, and
declining distributions of the remaining 14 species. These figures
provide evidence for widespread concern of native aquatic communities
of this region, in particular for habitat and prey species of northern
Mexican gartersnakes. Some conservation value, however, is realized
when headwaters, springs, and small streams are protected as parks or
municipal water supplies (Lyons et al. 1998, p. 15), but these efforts
do little to protect larger perennial rivers that represent valuable
habitat for northern Mexican gartersnakes.
Mercado-Silva et al. (2002, Appendix 2) reported results from fish
community sampling and habitat assessments along 63 sites across
central Mexico, the eastern-most of which include most of the northern
Mexican gartersnakes' southern range. Specifically, sampling locations
in the Balsas, Lerma, Morelia, P[aacute]nuco Moctezuma, and
P[aacute]nuco Tampa[oacute]n basins each occurred within the range of
the northern Mexican gartersnake in the states of Guanajuato,
[[Page 41533]]
Queretaro, Mexico, and Puebla; approximately 30 locations in total. The
purpose of this sampling effort was to score each site in terms of its
index of biotic integrity (IBI) and environmental quality (EQ), with a
score of 100 representing the optimum score for each category. The IBI
scoring method has been verified as a valid means to quantitatively
assess ecosystem integrity at each site (Lyons et al. 1995, pp. 576-
581; Mercado-Silva et al. 2002, p. 184). The range in IBI scores in
these sampling locations was 85 to 35, and the range in EQ scores was
90 to 50 (Mercado-Silva et al. 2002, Appendix 2). The average IBI score
was 57, and the average EQ score was 74, across all 30 sites and all
four basins (Mercado-Silva et al. 2002, Appendix 2). According to the
qualitative equivalencies assigned to scores (Mercado-Silva et al.
2002, p. 184), these values indicate that the environmental quality
score averaged across all 30 sites was ``good'' and the biotic
integrity scores were ``fair.'' It should be noted that 14 of the 30
sites sampled had IBI scores equal to or less than 50, and five of
those ranked as ``poor.'' Of all the basins throughout central Mexico
that were scored in this exercise, the two P[aacute]nuco basins
represented 20 of the 30 sites sampled and scored the worst of all
basins (Mercado-Silva et al. 2002, p. 186). This indicates that threats
to the northern Mexican gartersnake, its prey base, and its habitat
pose the greatest risk in this portion of its range in Mexico.
Near Torre[oacute]n, Coahuila, where the northern Mexican
gartersnake occurs, groundwater pumping has resulted in flow reversal,
which has dried up many local springs, drawn arsenic-laden water to the
surface, and resulted in adverse human health effects in that area
(Miller et al. 2005, p. 61). Severe water pollution from untreated
domestic waste is evident downstream of large Mexican cities, such as
Mexico City, and inorganic pollution from nearby industrialized areas
and agricultural irrigation return flow has dramatically affected
aquatic communities through contamination (Miller et al. 2005, p. 60).
Miller et al. (2005, p. 61) provide an excerpt from Soto Galera et al.
(1999) addressing the threats to the R[iacute]o Lerma, Mexico's longest
river, which is occupied by the northern Mexican gartersnake: ``The
basin has experienced a staggering amount of degradation during the
20th Century. By 1985-1993, over half of our study sites had
disappeared or become so polluted that they could no longer support
fishes. Only 15 percent of the sites were still capable of supporting
sensitive species. Forty percent (17 different species) of the native
fishes of the basin had suffered major declines in distribution, and
three species may be extinct. The extent and magnitude of degradation
in the R[iacute]o Lerma basin matches or exceeds the worst cases
reported for comparably sized basins elsewhere in the world.''
In the Transvolcanic Belt Region of the states of Jalisco, Mexico,
and Veracruz in southern Mexico, Conant (2003, p. 4) noted that water
diversions, pollution (e.g., discharge of raw sewage), sedimentation of
aquatic habitats, and increased dissolved nutrients were resulting in
decreased dissolved oxygen in suitable northern Mexican gartersnake
habitat. Conant (2003, p. 4) stated that many of these threats were
evident during his field work in the 1960s, and that they are
``continuing with increased velocity.''
High-Intensity Wildfires and Sedimentation of Aquatic Habitat
Low-intensity fire has been a natural disturbance factor in
forested landscapes for centuries, and low-intensity fires were common
in southwestern forests prior to European settlement (Rinne and Neary
1996, pp. 135-136). Rinne and Neary (1996, p. 143) discuss effects of
recent fire management policies on aquatic communities in Madrean Oak
Woodland biotic communities in the southwestern United States. They
concluded that existing wildfire suppression policies intended to
protect the expanding number of human structures on forested public
lands have altered the fuel loads in these ecosystems and increased the
probability of high-intensity wildfires. The effects of these high-
intensity wildfires include the removal of vegetation, the degradation
of subbasin condition, altered stream behavior, and increased
sedimentation of streams. These effects can harm fish communities, as
observed in the 1990 Dude Fire, when corresponding ash flows resulted
in fish kills in Dude Creek and the East Verde River (Voeltz 2002, p.
77). Fish kills, also discussed below, can drastically affect the
suitability of habitat for northern Mexican and narrow-headed
gartersnakes due to the removal of a portion or the entire prey base.
The Chiricahua leopard frog recovery plan cites altered fire regimes as
a serious threat to Chiricahua leopard frogs, a prey species for
northern Mexican gartersnakes (USFWS 2007, pp. 38-39).
The nature and occurrence of wildfires in the Southwest is expected
to also be affected by climate change and ongoing drought. Current
predictions of drought and/or higher winter low temperatures may stress
ponderosa pine forests in which the narrow-headed gartersnake
principally occurs, and may increase the frequency and magnitude of
wildfire. Ganey and Vojta (2010, entire) studied tree mortality in
mixed conifer and ponderosa pine forests in Arizona from 1997-2007, a
period of extreme drought. They found the mortality of trees to be
severe; the number of trees dying over a 5[hyphen]year period increased
by over 200 percent in mixed[hyphen]conifer forest and by 74 percent in
ponderosa pine forest during this time frame. Ganey and Vojta (2010)
attributed drought and subsequent insect (bark beetle) infestation to
the die-offs in trees. Drought stress and a subsequent high degree of
tree mortality from bark beetles make high-elevation forests more
susceptible to high-intensity wildfires. Climate is a top-down factor
that synchronizes with fuel loads, a bottom-up factor. Combined with a
predicted reduction in snowpack and an earlier snowmelt, these factors
suggest wildfires will be larger, more frequent, and more severe in the
southwestern United States (Ful[eacute] 2010). Wildfires are expected
to reduce vegetative cover and result in greater soil erosion,
subsequently resulting in increased sediment flows in streams
(Ful[eacute] 2010, entire). Increased sedimentation in streams reduces
the visibility of gartersnakes in the water column, hampering their
hunting ability as well as resulting in fish kills (which is also
caused by the disruption in the nitrogen cycle post-wildfire), which
reduce the amount of prey available to gartersnake populations.
Additionally, unnaturally high amounts of sediment fill in pools in
intermittent streams, which reduces the amount and availability of
habitat for fish and amphibian prey.
In the last 2 years, both Arizona (2011 Wallow Fire) and New Mexico
(2012 Whitewater-Baldy Complex Fire) have experienced the largest
wildfires in their respective State histories; indicative of the last
decade that has been punctuated by wildfires of massive proportion. The
2011 Wallow Fire consumed approximately 540,000 acres (218,530 ha) of
Apache-Sitgreaves National Forest, White Mountain Apache Indian Tribe,
and San Carlos Apache Indian Reservation lands in Apache, Navajo,
Graham, and Greenlee counties in Arizona as well as Catron County, New
Mexico (InciWeb 2011). The 2011 Wallow Fire impacted 97 percent of
perennial streams in the Black River subbasin, 70 percent of perennial
streams in the Gila River subbasin, and
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78 percent of the San Francisco River subbasin and resulted in
confirmed fish kills in each subbasin (Meyer 2011; p. 3, Table 2); each
of these streams is known to support populations of either northern
Mexican or narrow-headed gartersnakes.
Although the Black River drainage received no moderate or high-
severity burns as a result of the 2011 Wallow Fire, the Fish and Snake
Creek subbasins (tributaries to the Black River) were severely burned
(Coleman 2011, p. 2). Post-fire fisheries surveys above Wildcat Point
in the Black River found no fish in a reach extending up to the
confluence with the West Fork of Black River. This was likely due to
subsequent ash and sediment flows that had occurred there (Coleman
2011, p. 2). Post-fire fisheries surveys at ``the Box,'' in the Blue
River, detected only a single native fish. This was also likely due to
ash and sediment flows and the associated subsequent fish kills that
had occurred there, extending down to the Gila River Box in Safford,
Arizona (Coleman 2011, pp. 2-3). The East Fork Black River subbasin
experienced moderate to high-severity burns in 23 percent of its total
acreage that resulted in declines in Apache trout and native sucker
populations, but speckled dace and brown trout remained prevalent as of
2011 (Coleman 2011, p. 3). These fire data suggest that the persistence
of the prey base for northern Mexican and narrow-headed gartersnakes in
the Black River, and narrow-headed gartersnakes in the lower Blue
River, will be precarious into the near- to midterm future, as will
likely be the stability of gartersnake populations there.
Several large wildfires, which have resulted in excessive
sedimentation of streams and affected resident fish populations that
serve as prey for narrow-headed gartersnakes, have occurred
historically on the Gila National Forest. From 1989-2004, numerous
wildfires cumulatively burned much of the uplands within the Gila
National Forest, which resulted in most perennial streams in the area
experiencing ash flows and elevated sedimentation (Paroz et al. 2006,
p. 55). More recently, the 2012 Whitewater-Baldy Complex Fire in the
Gila National Forest in New Mexico is the largest wildfire in that
State's history. This wildfire was active for more than 5 weeks and
consumed approximately 300,000 acres (121,406 ha) of ponderosa, mixed
conifer, pinyon-juniper, and grassland habitat (InciWeb 2012). Over 25
percent of the burn area experienced high-moderate burn severity
(InciWeb 2012) and included several subbasins occupied by narrow-headed
gartersnakes such as the Middle Fork Gila River, West Fork Gila River,
Iron Creek, the San Francisco River, Whitewater Creek, and Mineral
Creek (Brooks 2012, Table 1). Other extant populations of the narrow-
headed gartersnake in Gilita and South Fork Negrito Creeks are also
expected to be impacted from the 2012 Whitewater-Baldy Complex Fire.
Narrow-headed gartersnake populations in the Middle Fork Gila River and
Whitewater Creek formerly represented two of the four most robust
populations known from New Mexico, and two of the five known rangewide,
and are expected to have been severely jeopardized by post-fire effects
to their prey base. Thus, we now consider them currently as likely not
viable, at least in the short to medium term. In reference to Gila
trout populations, Brooks (2012, p. 3) stated that fish populations are
expected to be severely impacted in the West Fork Gila River and
Whitewater Creek. The loss of fish communities in affected streams is
likely to lead to associated declines, or potential extirpations, in
affected narrow-headed gartersnake populations as a result of the
collapse in their prey base.
Since 2000, several wildfires have affected occupied narrow-headed
gartersnake habitat on the Gila National Forest. The West Fork Gila
subbasin was affected by the 2002 Cub Fire, the 2003 Dry Lakes Fire,
and the 2011 Miller Fire; each resulted in post-fire ash and sediment
flows, which adversely affected fish populations used by narrow-headed
gartersnakes (Hellekson 2012a, pers. comm.). In 2011, the Miller Fire
significantly affected the Little Creek subbasin and has resulted in
substantive declines in abundance of the fish community (Hellekson
2012a, pers. comm.). Dry Blue and Campbell Blue creeks were affected by
the 2011 Wallow Fire (Hellekson 2012a, pers. comm.). Saliz Creek was
highly affected by the 2006 Martinez Fire (Hellekson 2012a, pers.
comm.). Turkey Creek was heavily impacted by the Dry Lakes Fire in
2002, which resulted in a complete fish kill, but the fish community
has since rebounded (Hellekson 2012a, pers. comm.). It is not certain
how long the fish community was sparse or absent from Turkey Creek, but
it is suspected that the narrow-headed gartersnake population there
suffered significant declines from the loss of their prey base, as
evidenced by the current low population numbers. Prior to the 2002 Dry
Lakes Fire, Turkey Creek was largely populated by nonnative, spiny-
rayed fish species, but has since been recolonized by native fish
species almost exclusively (Hellekson 2012a, pers. comm.), and may
provide high-quality habitat for narrow-headed gartersnakes, once the
subbasin has adequately stabilized.
Affects to northern Mexican and narrow-headed gartersnake habitat
from wildfire should be considered in light of effects to the
structural habitat and effects to the prey base. Post-fire effects vary
with burn severity, percent of area burned within each severity
category, and the intensity and duration of precipitation events that
follow (Coleman 2011, p. 4). Low-severity burns within riparian habitat
can actually have a rejuvenating effect by removing decadent ground
cover and providing nutrients to remaining vegetation. As a result,
riparian vegetative communities may be more resilient to wildfire,
given that water is present (Coleman 2011, p. 4). Willows, an important
component to narrow-headed gartersnake habitat, can be positively
affected by low-severity burns, as long as the root crowns are not
damaged (Coleman 2011, p. 4). High severity burns that occur within the
floodplain of occupied habitat are expected to have some level of
shorter-term effect on resident gartersnake populations through effects
to the vegetative structure and abundance, which may include a
reduction of basking sites and a loss of cover, which could increase
the risk of predation. These potential effects need further study.
Post-fire ash flows, flooding, and impacts to native prey populations
are longer term effects and can occur for many years after a large
wildfire (Coleman 2011, p. 2).
Post-fire flooding with significant ash and sediment loads can
result in significant declines, or even the collapse, of resident fish
communities, which poses significant concern for the persistence of
resident gartersnake populations in affected areas. Sedimentation can
adversely affect fish populations used as prey by northern Mexican or
narrow-headed gartersnakes by: (1) Interfering with respiration; (2)
reducing the effectiveness of fish's visually based hunting behaviors;
and (3) filling in interstitial (spaces between cobbles, etc., on the
stream floor) spaces of the substrate, which reduces reproduction and
foraging success of fish (Wheeler et al. 2005, p. 145). Excessive
sediment also fills in intermittent pools required for amphibian prey
reproduction and foraging. Siltation of the rocky interstitial spaces
along stream bottoms decreases the dissolved oxygen content where fish
lay their eggs, resulting in depressed recruitment of fish and a
[[Page 41535]]
subsequent reduction in prey abundance for northern Mexican and narrow-
headed gartersnakes through the loss of prey microhabitat (Nowak and
Santana-Bendix 2002, pp. 37-38). As stated above, sediment can lead to
several effects in resident fish species used by northern Mexican or
narrow-headed gartersnakes as prey, which can ultimately cause
increased direct mortality, reduced reproductive success, lower overall
abundance, and reductions in prey species composition as documented by
Wheeler et al. (2005, p. 145). The underwater foraging ability of
narrow-headed gartersnakes (de Queiroz 2003, p. 381) and likely
northern Mexican gartersnakes is largely based on vision and is also
directly compromised by excessive turbidity caused by sedimentation of
water bodies. Suspended sediment in the water column may reduce the
narrow-headed gartersnake's visual hunting efficiency from effects to
water clarity, based on research conducted by de Queiroz (2003, p. 381)
that concluded the species relied heavily on visual cues during
underwater striking behaviors.
The presence of adequate interstitial spaces along stream floors
may be particularly important for narrow-headed gartersnakes. Hibbitts
and Fitzgerald (2009, p. 464) reported the precipitous decline of
narrow-headed gartersnakes in a formerly robust population in the San
Francisco River at San Francisco Hot Springs from 1996 to 2004. The
exact cause for this significant decline is uncertain, but the
investigators suspected that a reduction in interstitial spaces along
the stream floor from an apparent conglomerate, cementation process may
have affected the narrow-headed gartersnake's ability to successfully
anchor themselves to the stream bottom when seeking refuge or foraging
for fish (Hibbitts and Fitzgerald 2009, p. 464). These circumstances
would likely result in low predation success and eventually starvation.
Other areas where sedimentation has affected either northern Mexican or
narrow-headed gartersnake habitat are Cibecue Creek in Arizona, and the
San Francisco River and South Fork Negrito Creek in New Mexico (Rosen
and Schwalbe 1988, p. 46; Arizona Department of Water Resources 2011,
p. 1; Hellekson 2012a, pers. comm.). The San Francisco River in Arizona
was classified as impaired due to excessive sediment from its
headwaters downstream to the Arizona-New Mexico border (Arizona
Department of Water Resources 2011, p. 1). South Fork Negrito Creek is
also listed as impaired due to excessive turbidity (Hellekson 2012a,
pers. comm.).
Summary--The presence of water is critical to both northern Mexican
and narrow-headed gartersnakes and their primary prey species because
their ecology and natural histories are strongly linked to water.
Several factors, both natural and manmade, contribute to the continued
degradation and dewatering of aquatic habitat throughout the range of
northern Mexican and narrow-headed gartersnakes. Increasing human
population growth is driving higher and higher demands for water in
both the United States and Mexico. Water is subsequently secured
through dams, diversions, flood-control projects, and groundwater
pumping, which affects gartersnake habitat through reductions in flow
and complete dewatering of stream reaches. Entire reaches of the Gila,
Salt, Santa Cruz, and San Francisco Rivers, as well as numerous other
rivers throughout the Mexican Plateau in Mexico which were historically
occupied by either or both northern Mexican or narrow-headed
gartersnakes, are now completely dry due to diversions, dams, and
groundwater pumping. Several groundwater basins within the range of
northern Mexican and narrow-headed gartersnakes in the United States
are considered active management areas where pumping exceeds recharge,
which is a constant threat to surface flow in streams and rivers
connected to these aquifers. Reduced flows concentrate northern Mexican
and narrow-headed gartersnakes and their prey with harmful nonnative
species, which accelerate and amplify adverse effects of native-
nonnative community interactions. Where surface water persists,
increasing land development and recreation use adjacent to and within
riparian habitat has led to further reductions in stream flow, removal
or alteration of vegetation, and increased frequency of adverse human
interactions with gartersnakes.
Exacerbating the effects of increasing human populations and higher
water demands, climate change predictions include increased aridity,
lower annual precipitation totals, lower snow pack levels, higher
variability in flows (lower low-flows and higher high-flows), and
enhanced stress on ponderosa pine communities in the southwestern
United States and northern Mexico. Increased stress to ponderosa pine
forests places them at higher risk of high-intensity wildfires, the
effects of which are discussed below. Climate change has also been
predicted to enhance the abundance and distribution of harmful
nonnative species, which adversely affect northern Mexican and narrow-
headed gartersnakes.
Cienegas, a unique and important habitat for northern Mexican
gartersnakes, have been adversely affected or eliminated by a variety
of historical and current land uses in the United States and Mexico,
including streambed modification, intensive livestock grazing,
woodcutting, artificial drainage structures, stream flow stabilization
by upstream dams, channelization, and stream flow reduction from
groundwater pumping and water diversions. The historical loss of the
cienega habitat of the northern Mexican gartersnake has resulted in
local population declines or extirpations, negatively affecting its
status and contributing to its decline rangewide.
Wildfire has historically been a natural and important disturbance
factor within the range of northern Mexican and narrow-headed
gartersnakes. However, in recent decades, forest management policies in
the United States have favored fire suppression, the result of which
has led to wildfires of unusual proportions, particularly along the
Mogollon Rim of Arizona and New Mexico. These policies are generally
not in place in Mexico, and consequently, wildfire is not viewed as a
significant threat to the northern Mexican gartersnake in Mexico.
However, in the last 2 years, both Arizona (2011 Wallow Fire) and New
Mexico (2012 Whitewater-Baldy Complex Fire) have experienced the
largest wildfires in their respective State histories, which is
indicative of the last decade having been punctuated by wildfires of
significant magnitude. High-intensity wildfire has been shown to result
in significant ash and sediment flows into habitat occupied by northern
Mexican or narrow-headed gartersnakes, resulting in significant
reductions of their fish prey base and, in some instances, total fish
kills. The interstitial spaces between rocks located along the stream
floor are important habitat for the narrow-headed gartersnake as a
result of its specialized foraging strategy and specialized diet. They
area also important for several fish species relied upon as prey. When
these spaces fill in with sediment, the narrow-headed gartersnake may
be unable to forage successfully and may succumb to stress created by a
depressed prey base. A significant reduction or absence of a prey base
results in stress of resident gartersnake populations and can result in
local population extirpations. Also, narrow-headed gartersnakes are
believed to rely heavily on visual cues
[[Page 41536]]
while foraging underwater; increased turbidity from suspended fine
sediment in the water column is likely to impede their ability to use
visual cues at some level. Factors that result in depressed foraging
ability from excessive sedimentation are likely to be enhanced when
effects from harmful nonnative species are also acting on resident
northern Mexican and narrow-headed gartersnake populations. We consider
the narrow-headed gartersnake to be particularly threatened by the
effects of wildfires as described because they occur throughout its
range, the species is a fish-eating specialist that is unusually
vulnerable to localized fish kills, and wildfire has already
significantly affected two of the last remaining five populations that
were formerly considered viable, pre-fire. We have demonstrated that
high-intensity wildfires have the potential to eliminate gartersnake
populations through a reduction or loss of their prey base. Since 1970,
wildfires have adversely impacted the native fish prey base in 6
percent of the historical distribution of northern Mexican gartersnakes
in the United States and 21 percent of that for narrow-headed
gartersnakes rangewide, according to GIS analysis.
All of these conditions affect the primary drivers of gartersnake
habitat suitability (the presence of water and prey) and exist in
various degrees throughout the range of both gartersnake species.
Collectively, they reduce the amount and arrangement of physically
suitable habitat for northern Mexican and narrow-headed gartersnakes
over their regional landscapes. The genetic representation of each
species is threatened when populations become disconnected and isolated
from neighboring populations because the length or area of dewatered
zones is too great for dispersing individuals to overcome. Therefore,
normal colonizing mechanisms that would otherwise reestablish
populations where they have become extirpated are no longer viable.
This subsequently leads to a reduction in species redundancy when
isolated, small populations are at increased vulnerability to the
effects of stochastic events, without a means for natural
recolonization. Ultimately, the effects of scattered, small, and
disjunct populations, without the means to naturally recolonize, is
weakened species resiliency as a whole, which ultimately enhances the
risk of either or both species becoming endangered or going extinct.
Therefore, based on the best available scientific and commercial
information, we conclude that land uses or conditions described above
that alter or dewater northern Mexican and narrow-headed gartersnake
habitat are threats rangewide, now and in the foreseeable future.
The Cumulative and Synergistic Effect of Threats on Low-Density
Northern Mexican and Narrow-Headed Gartersnake Populations
In most locations where northern Mexican or narrow-headed
gartersnakes historically occurred or still occur currently, two or
more threats are likely acting in combination with regard to their
influence on the suitability of those habitats or on the species
themselves. Many threats could be considered minor in isolation, but
when they affect gartersnake populations in combination with other
threats, become more serious. We have concluded that in as many as 24
of 29 known localities in the United States (83 percent), the northern
Mexican gartersnake population is likely not viable and may exist at
low population densities that could be threatened with extirpation or
may already be extirpated. We also determined that in as many as 29 of
38 known localities (76 percent), the narrow-headed gartersnake
population is likely not viable and may exist at low population
densities that could be threatened with extirpation or may already be
extirpated but survey data are lacking in areas where access is
restricted. We have also discussed how harmful nonnative species have
affected recruitment of gartersnakes across their range. In viable
populations, gartersnakes are resilient to the loss of individuals
through ongoing recruitment into the reproductive age class. However,
when northern Mexican or narrow-headed gartersnakes occur at low
population densities in the absence of appropriate recruitment, the
loss of even a few adults, or even a single adult female, could drive a
local population to extirpation. Below, we discuss threats that, when
considered in combination, can appreciably threaten low-density
populations with extirpation.
Historical and Unmanaged Livestock Grazing and Agricultural Land Uses
Currently in the United States, livestock grazing is a largely
managed activity, but in Mexico, livestock grazing is much less managed
or unmanaged altogether. The effect of livestock grazing on resident
gartersnake populations must be examined as a comparison between
historical and current management, and in the presence of harmful
nonnative species, or not. Historical livestock grazing has damaged
approximately 80 percent of stream, cienega, and riparian ecosystems in
the western United States (Kauffman and Krueger 1984, pp. 433-435;
Weltz and Wood 1986, pp. 367-368; Cheney et al. 1990, pp. 5, 10; Waters
1995, pp. 22-24; Pearce et al. 1998, p. 307; Belsky et al. 1999, p. 1).
Fleischner (1994, p. 629) found that ``Because livestock congregate in
riparian ecosystems, which are among the most biologically rich
habitats in arid and semiarid regions, the ecological costs of grazing
are magnified at these sites.'' Stromberg and Chew (2002, p. 198) and
Trimble and Mendel (1995, p. 243) also discussed the propensity for
cattle to remain within or adjacent to riparian communities.
Expectedly, this behavior is more pronounced in more arid regions
(Trimble and Mendel 1995, p. 243). Effects from historical or unmanaged
grazing include: (1) Declines in the structural richness of the
vegetative community; (2) losses or reductions of the prey base; (3)
increased aridity of habitat; (4) loss of thermal cover and protection
from predators; (5) a rise in water temperatures to levels lethal to
larval stages of amphibian and fish development; and (6)
desertification (Szaro et al. 1985, p. 362; Schulz and Leininger 1990,
p. 295; Schlesinger et al. 1990, p. 1043; Belsky et al. 1999, pp. 8-11;
Zwartjes et al. 2008, pp. 21-23). In one rangeland study, it was
concluded that 81 percent of the vegetation that was consumed,
trampled, or otherwise removed was from a riparian area, which amounted
to only 2 percent of the total grazing space, and that these actions
were 5 to 30 times higher in riparian areas than on the uplands
(Trimble and Mendel 1995, pp. 243-244). However, according to one study
along the Agua Fria River, herbaceous ground cover can recover quickly
from heavy grazing pressure (Szaro and Pase 1983, p. 384). Additional
information on the effects of historical livestock grazing can be found
in Sartz and Tolsted (1974, p. 354); Rosen and Schwalbe (1988, pp. 32-
33, 47); Clary and Webster (1989, p. 1); Clary and Medin (1990, p. 1);
Orodho et al. (1990, p. 9); and Krueper et al. (2003, pp. 607, 613-
614).
Szaro et al. (1985, p. 360) assessed the effects of historical
livestock management on a sister taxon and found that western
(terrestrial) gartersnake (Thamnophis elegans vagrans) populations were
significantly higher (versus controls) in terms of abundance and
biomass in areas that were excluded from grazing, where the streamside
vegetation remained lush, than where uncontrolled access to grazing was
permitted. This effect was
[[Page 41537]]
complemented by higher amounts of cover from organic debris from
ungrazed shrubs that accumulate as the debris moves downstream during
flood events. Specifically, results indicated that snake abundance and
biomass were significantly higher in ungrazed habitat, with a five-fold
difference in number of snakes captured, despite the difficulty of
making observations in areas of increased habitat complexity (Szaro et
al. 1985, p. 360). Szaro et al. (1985, p. 362) also noted the
importance of riparian vegetation for the maintenance of an adequate
prey base and as cover in thermoregulation and predation avoidance
behaviors, as well as for foraging success. Direct mortality of
amphibian species, in all life stages, from being trampled by livestock
has been documented in the literature (Bartelt 1998, p. 96; Ross et al.
1999, p. 163). Gartersnakes may, on occasion, be trampled by livestock.
A black-necked gartersnake (Thamnophis cyrtopsis cyrtopsis) had
apparently been killed by livestock trampling along the shore of a
stock tank in the Apache-Sitgreaves National Forest, within an actively
grazed allotment (Chapman 2005).
Subbasins where historical grazing has been documented as a
suspected contributing factor for either northern Mexican or narrow-
headed gartersnake declines include the Verde, Salt, Agua Fria, San
Pedro, Gila, and Santa Cruz (Hendrickson and Minckley 1984, pp. 140,
152, 160-162; Rosen and Schwalbe 1988, pp. 32-33; Girmendonk and Young
1997, p. 47; Hale 2001, pp. 32-34, 50, 56; Voeltz 2002, pp. 45-81;
Krueper et al. 2003, pp. 607, 613-614; Forest Guardians 2004, pp. 8-10;
Holycross et al. 2006, pp. 52-61; McKinnon 2006d, 2006e; Paradzick et
al. 2006, pp. 90-92; USFS 2008). Livestock grazing still occurs in
these subbasins but is a largely managed land use and is not likely to
pose significant threats to either northern Mexican or narrow-headed
gartersnakes where closely managed. In cases where poor livestock
management results in fence lines in persistent disrepair, providing
unmanaged livestock access to occupied habitat, adverse effects from
loss of vegetative cover may result, most likely in the presence of
harmful nonnative species. As we described above, however, we strongly
suspect that northern Mexican and narrow-headed gartersnakes are
somewhat resilient to physical habitat disturbance where harmful
nonnative species are absent.
The creation and maintenance of stock tanks is an important
component to livestock grazing in the southwestern United States. Stock
tanks associated with livestock grazing may facilitate the spread of
harmful nonnative species when they are intentionally or
unintentionally stocked by anglers and private landowners (Rosen et al.
2001, p. 24). The management of stock tanks is an important
consideration for northern Mexican gartersnakes in particular. Stock
tanks associated with livestock grazing can be intermediary ``stepping
stones'' in the dispersal of nonnative species from larger source
populations to new areas (Rosen et al. 2001, p. 24). The effects of
livestock grazing at stock tanks on northern Mexican gartersnakes
depend on how they are managed. Dense bank and aquatic vegetation is an
important habitat characteristic for the northern Mexican gartersnake
in the presence of harmful nonnative species. This vegetation can be
affected if the impoundment is poorly managed. When harmful nonnative
species are absent, the presence of bank line vegetation is less
important. Well-managed stock tanks provide important habitat for
northern Mexican gartersnakes and their prey base, especially when the
tank: (1) Remains devoid of harmful nonnative species while supporting
native prey species; (2) provides adequate vegetation cover; and (3)
provides reliable water sources in periods of prolonged drought. Given
these benefits of well-managed stock tanks, we believe well-managed
stock tanks are an important, even vital, component to northern Mexican
gartersnake conservation and recovery.
Road Construction, Use, and Maintenance
Roads can pose unique threats to herpetofauna, and specifically to
species like the northern Mexican gartersnake, its prey base, and the
habitat where it occurs. The narrow-headed gartersnake, alternatively,
is probably less affected by roads due to its more aquatic nature.
Roads fragment occupied habitat and can result in diminished genetic
viability in populations from increased mortality from vehicle strikes
and adverse human encounters as supported by current research on
eastern indigo snakes (Breininger et al. 2012, pp. 364-366). Roads
often track along streams and present a mortality risk to gartersnakes
seeking more upland, terrestrial habitat for brumation and gestation.
Roads may cumulatively impact both species through the following
mechanisms: (1) Fragmentation, modification, and destruction of
habitat; (2) increase in genetic isolation; (3) alteration of movement
patterns and behaviors; (4) facilitation of the spread of nonnative
species via human vectors; (5) an increase in recreational access and
the likelihood of subsequent, decentralized urbanization; (6)
interference with or inhibition of reproduction; (7) contributions of
pollutants to riparian and aquatic communities; (8) reduction of prey
communities; (9) effects to gartersnake reproduction; and (10) acting
as population sinks (when population death rates exceed birth rates in
a given area) (Rosen and Lowe 1994, pp. 146-148; Waters 1995, p. 42;
Foreman and Alexander 1998, p. 220; Trombulak and Frissell 2000, pp.
19-26; Carr and Fahrig 2001, pp. 1074-1076; Hels and Buchwald 2001, p.
331; Smith and Dodd 2003, pp. 134-138; Angermeier et al. 2004, pp. 19-
24; Shine et al. 2004, pp. 9, 17-19; Andrews and Gibbons 2005, pp. 777-
781; Wheeler et al. 2005, pp. 145, 148-149; Roe et al. 2006, p. 161;
Sacco 2007, pers. comm.; Ouren et al. 2007, pp. 6-7, 11, 16, 20-21;
Jones et al. 2011, pp. 65-66; Hellekson 2012a, pers. comm.).
Perhaps the most common factor in road mortality of snakes is the
propensity for drivers to unintentionally and intentionally run them
over, both because people tend to dislike snakes (Rosen and Schwalbe
1988, p. 43; Ernst and Zug 1996, p. 75; Green 1997, pp. 285-286; Nowak
and Santana-Bendix 2002, p. 39) and because they make easy targets
crossing roads at perpendicular angles (Klauber 1956, p. 1026; Langley
et al. 1989, p. 47; Shine et al. 2004, p. 11). Mortality data for
northern Mexican gartersnakes have been collected at the Bubbling Ponds
Hatchery since 2006. Of the 15 dead specimens, eight were struck by
vehicles on roads within or adjacent to the hatchery ponds, perhaps
while crossing between ponds to forage (Boyarski 2011, pp. 1-3). Van
Devender and Lowe (1977, p. 47), however, observed several northern
Mexican gartersnakes crossing the road at night after the commencement
of the summer monsoon (rainy season), which highlights the seasonal
variability in surface activity of this snake. Wallace et al. (2008,
pp. 243-244) documented a vehicle-related mortality of a northern
Mexican gartersnake on Arizona State Route 188 near Tonto Creek that
occurred in 1995.
Adverse Human Interactions With Gartersnakes
A fear of snakes is generally and universally embedded in modern
culture, and is prevalent in the United States (Rosen and Schwalbe
1988, p. 43; Ernst and Zug 1996, p. 75; Green 1997, pp. 285-286; Nowak
and Santana-Bendix 2002, p. 39). We use the phrase ``adverse human
interaction'' to refer to the act of humans directly injuring or
[[Page 41538]]
killing snakes out of a sense of fear or anxiety (ophidiophobia), or
for no apparent purpose. One reason the narrow-headed gartersnake is
vulnerable to adverse human interactions is because of its appearance.
The narrow-headed gartersnake is often confused for a venomous water
moccasin (cottonmouth, Agkistrodon piscivorus), because of its
triangular-shaped head and propensity to be found in or near water
(Nowak and Santana-Bendix 2002, p. 38). Although the nearest water
moccasin populations are located over 700 miles (1,127 km) to the east
in central Texas, these misidentifications prove fatal for narrow-
headed gartersnakes (Nowak and Santana-Bendix 2002, p. 38).
Adverse human interaction may be largely responsible for highly
localized extirpations in narrow-headed gartersnakes based on the
collection history of the species at Slide Rock State Park along Oak
Creek, where high recreation use is strongly suspected to result in
direct mortality of snakes by humans (Nowak and Santana-Bendix 2002,
pp. 21, 38). Rosen and Schwalbe (1988, p. 42-43) suggested that
approximately 44 percent of the estimated annual mortality of narrow-
headed gartersnakes in the larger size classes along Oak Creek may be
human-caused. Declines in narrow-headed gartersnake populations in the
North and East Forks of the White River have also been attributed to
humans killing snakes (Rosen and Schwalbe 1988, pp. 43-44). Locations
in New Mexico where this unnatural form of mortality is believed to
have historically affected or currently affect narrow-headed
gartersnakes include Wall Lake (Fleharty 1967, p. 219), Middle Fork of
the Gila River, the mainstem Gila River from Cliff Dwellings to Little
Creek, in Whitewater Creek from the Catwalk to Glenwood (L. Hellekson
2012a, pers. comm.), and near San Francisco Hot Springs along the San
Francisco River (Hibbitts and Fitzgerald 2009, p. 466).
Environmental Contaminants
Environmental contaminants, such as heavy metals, may be common at
low background levels in soils and, as a result, concentrations are
known to bioaccumulate in food chains. A bioaccumulative substance
increases in concentration in an organism or in the food chain over
time. A mid- to higher-order predator, such as a gartersnake, may,
therefore, accumulate these types of contaminants over time in their
fatty tissues, which may lead to adverse health effects (Wylie et al.
2009, p. 583, Table 5). Campbell et al. (2005, pp. 241-243) found that
metal concentrations accumulated in the northern watersnake (Nerodia
sipedon) at levels six times that of their primary prey item, the
central stoneroller (a fish, Campostoma anomalum). Metals, in trace
amounts, can be sequestered in the skin of snakes (Burger 1999, p.
212), interfere with metabolic rates of snakes (Hopkins et al. 1999, p.
1261), affect the structure and function of their liver and kidneys,
and may also act as neurotoxins, affecting nervous system function
(Rainwater et al. 2005, p. 670). Based on data collected in 2002-2010,
mercury appears to be bioaccumulating in fish found in the lower
reaches of Tonto Creek, where northern Mexican gartersnakes also occur
(Rector 2010, pers. comm.). In fact, the State record for the highest
mercury concentrations in fish tissue was reported in Tonto Creek from
this investigation by Rector (2010, pers. comm.). Mercury levels were
found to be the highest in the piscivorous smallmouth bass and,
secondly, in desert suckers (a common prey item for northern Mexican
and narrow-headed gartersnakes). Because gartersnakes eat fish, mercury
may be bioaccumulating in resident populations, although no testing has
occurred.
Specific land uses such as mining and smelting, as well as road
construction and use, can be significant sources of contaminants in
air, water, or soil through point-source and non-point source
mechanisms. Copper mining has occurred in Arizona (Pima, Pinal,
Yavapai, and Gila Counties) and adjacent Mexico for centuries, and many
of these sites have smelters (now decommissioned), which are former
sources of airborne contaminants. The mining industry in Mexico is
largely concentrated in the northern tier of that country, with the
State of Sonora being the leading producer of copper, gold, graphite,
molybdenum, and wollastonite, as well as the leader among Mexican
States with regard to the amount of surface area dedicated to mining
(Stoleson et al. 2005, p. 56). The three largest mines in Mexico (all
copper) are found in Sonora (Stoleson et al. 2005, p. 57). The sizes of
mines in Sonora vary considerably, as do the known environmental
effects from mining-related activities (from exploration to long after
closure), which include contamination and drawdown of groundwater
aquifers, erosion, acid mine drainage, fugitive dust, pollution from
smelter emissions, and landscape clearing (Stoleson et al. 2005, p.
57). We are aware of no specific research on potential effects of
mining or environmental contaminants acting on northern Mexican
gartersnakes in Mexico, but presume, based on the best available
scientific and commercial information, that where this land use is
prevalent, contaminants may be a contributing threat to resident
gartersnakes or their prey.
Northern Mexican Gartersnake Competition With Marcy's Checkered
Gartersnake
Preliminary research suggests that Marcy's checkered gartersnake
(Thamnophis marcianus marcianus) may impact the future conservation of
the northern Mexican gartersnake in southern Arizona, although
supporting data are limited. Rosen and Schwalbe (1988, p. 31)
hypothesized that bullfrogs are more likely to eliminate northern
Mexican gartersnakes when Marcy's checkered gartersnakes are also
present. Marcy's checkered gartersnake is a semi-terrestrial species
that is able to co-exist to some degree with harmful nonnative
predators. This might be due to its apparent ability to forage in more
terrestrial habitats, specifically during the vulnerable juvenile size
classes (Rosen and Schwalbe 1988, p. 31; Rosen et al. 2001, pp. 9-10).
In every age class, the northern Mexican gartersnake forages in aquatic
habitats where nonnative spiny-rayed fish, bullfrogs, and crayfish are
present, which increases not only the encounter rate between predator
and prey, but also the juvenile mortality rate of the northern Mexican
gartersnake, which negatively affects recruitment. As northern Mexican
gartersnake numbers decline within a population, space becomes
available for occupation by Marcy's checkered gartersnakes. One
hypothesis suggests that the Marcy's checkered gartersnake might affect
the maximum number of northern Mexican gartersnakes that an area can
maintain based upon available resources, and could potentially
accelerate the decline of, or preclude re-occupancy by, the northern
Mexican gartersnake (Rosen and Schwalbe 1988, p. 31). Rosen et al.
(2001, pp. 9-10) documented the occurrence of Marcy's checkered
gartersnakes replacing northern Mexican gartersnakes at the San
Bernardino National Wildlife Refuge and surrounding habitats of the
Black Draw. Rosen and Schwalbe (1988, p. 31) report the same at the
mouth of Potrero Canyon near its confluence with the lower Santa Cruz
River. They suspected that drought, extending from the late 1980s
through the late 1990s, played a role in the degree of competition for
aquatic resources, provided an advantage to the more versatile Marcy's
checkered gartersnake, and expedited
[[Page 41539]]
the decline of the northern Mexican gartersnake. More research is
needed to confirm these relationships.
Mortality From Entanglement Hazards
In addressing the effects of soil erosion associated with road
construction projects or post-fire remedial subbasin management,
erosion control materials placed on the ground surface are often used.
Erosion control is considered a best management practice for most soil-
disturbing activities, and is broadly required as mitigation across the
United States, in particular to avoid excess sedimentation of streams
and rivers. Rolled erosion control products, such as temporary erosion
control blankets and permanent turf reinforcement mats, are two methods
commonly used for these purposes (Barton and Kinkead 2005, p. 34).
These products use stitching or net-like mesh products to hold
absorbent media together. At a restoration site in South Carolina, 19
snakes (15 dead) representing five different species were found
entangled in the netting and had received severe lacerations in the
process of attempting to escape their entanglement (Barton and Kinkead
2005, p. 34). Stuart et al. (2001, pp. 162-164) also reported the
threats of net-like debris to snake species. Kapfer and Paloski (2011,
p. 4) reported at least 31 instances involving six different species of
snake (including the common gartersnake) in Wisconsin that had become
entangled in the netting used for either erosion control or as a
wildlife exclusion product. In their review, Kapfer and Paloski (2011,
p. 6) noted that 0.5 in. by 0.5 in. mesh has the greatest likelihood of
entangling snakes.
Similar snake mortalities have not been documented in Arizona or
New Mexico, according to our files. However, given the broad usage of
these materials across the distribution of the northern Mexican and
narrow-headed gartersnakes, it is not unlikely that mortality occurs
but goes unreported. The likelihood of either gartersnake species
becoming entangled depends on the distance these erosion control
materials are used from water in occupied habitat and the density of
potentially affected populations. Because erosion control products are
usually used to prevent sedimentation of streams, there is a higher
likelihood for gartersnakes to become entangled. This potential threat
will require public education and additional monitoring and research,
with emphasis in regions with occupied habitat.
Finally, discarded fishing nets have also been documented as a
source of mortality for northern Mexican gartersnakes in the area of
Lake Chapala, Jalisco, Mexico (Barrag[aacute]n-Ram[iacute]rez and
Ascencio-Arrayga 2013, p. 159). Netting or seining is not an authorized
form of recreational fishing for sport fish in Arizona or New Mexico,
but the practice is allowed in either state for the collection of live
baitfish (AGFD 2013, p. 57; NMDGF 2013, p. 17). We are not certain of
the frequency in which these techniques are used for such purposes in
either state, but do not suspect that discarded nets or seines are
commonly left on-site where they could ensnarl resident gartersnakes.
However, this practice is used in Mexico as a primary means of
obtaining freshwater fish as a food source and may be a significant
threat to local northern Mexican gartersnake populations where this
practice occurs.
Disease
Our review of the scientific literature did not find evidence that
disease is a current factor contributing to the decline in northern
Mexican or narrow-headed gartersnakes. However, a recent wildlife
health bulletin announced the emergence of snake fungal disease (SFD)
within the eastern and Midwestern portions of the United States
(Sleemen 2013, p. 1). SFD has now been diagnosed in several terrestrial
and aquatic snake genera including Nerodia, Coluber, Pantherophis,
Crotalus, Sistrurus, and Lampropeltis. Clinical signs of SFD include
scabs or crusty scales, subcutaneous nodules, abnormal molting, white
opaque cloudiness of the eyes, localized thickening or crusting of the
skin, skin ulcers, swelling of the face, or nodules in the deeper
tissues (Sleemen 2013, p. 1). While mortality has been documented as a
result of SFD, population-level impacts have not, due to the cryptic
and solitary nature of snakes and the lack of long-term monitoring data
(Sleemen 2013, p. 1). So far, no evidence of SFD has been found in the
genus Thamnophis but the documented occurrence of SFD in ecologically
similar, aquatic colubrids such as Nerodia is cause for concern. We
recommend resource managers remain diligent in looking for signs of SFD
in wild gartersnake populations.
Summary
We found numerous effects of livestock grazing that have resulted
in the historical degradation of riparian and aquatic communities that
have likely affected northern Mexican and narrow-headed gartersnakes.
The literature concluded that mismanaged or unmanaged grazing can have
disproportionate effects to riparian communities in arid ecosystems due
to the attraction of livestock to water, forage, and shade. We found
current livestock grazing activities to be more of a concern in Mexico.
The literature is clear that the most profound impacts from livestock
grazing in the southwestern United States occurred nearly 100 years
ago, were significant, and may still be affecting some areas that have
yet to fully recover. Unmanaged or poorly managed livestock operations
likely have more pronounced effects in areas significantly impacted by
harmful nonnative species through a reduction in cover. However, land
managers in Arizona and New Mexico currently emphasize the protection
of riparian and aquatic habitat in allotment management planning,
usually through fencing, rotation, monitoring, and range improvements
such as developing remote water sources. Collectively, these measures
have reduced the likelihood of significant adverse impacts on northern
Mexican or narrow-headed gartersnakes, their habitat, and their prey
base. We also recognize that while the presence of stock tanks on the
landscape can benefit nonnative species, well-managed stock tanks are
an invaluable tool in the conservation and recovery of northern Mexican
gartersnakes and their prey.
Other activities, factors, or conditions that act in combination,
such as road construction, use, and management, adverse human
interactions, environmental contaminants, entanglement hazards, and
competitive pressures from sympatric species, occur within the
distribution of these gartersnakes and have the propensity to
contribute to further population declines or extirpations where
gartersnakes occur at low population densities. An emerging skin
disease, SFD, has not yet been documented in gartersnakes but has
affected snakes of many genera within the United States, including
ecologically similar species, and may pose a future threat to northern
Mexican and narrow-headed gartersnakes. Where low density populations
are affected these types of threats described above, even the loss of a
few reproductive adults, especially females, from a population can have
significant population-level effects, most notably in the presence of
harmful nonnative species. Continued population declines and
extirpations threaten the genetic representation of each species
because many populations have become disconnected and isolated from
neighboring populations. This subsequently leads to a reduction in
species redundancy and resiliency
[[Page 41540]]
when isolated, small populations are at increased vulnerability to the
effects of stochastic events, without a means for natural
recolonization. Based on the best available scientific and commercial
information, we conclude these threats have the tendency to act
synergistically and disproportionately on low-density gartersnake
populations rangewide, now and in the foreseeable future.
The Inadequacy of Existing Regulatory Mechanisms
Below, we examine whether existing regulatory mechanisms are
inadequate to address the threats to the northern Mexican and narrow-
headed gartersnakes discussed under other factors. Section 4(b)(1)(A)
of the Endangered Species 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.'' We interpret this language to require us to consider
relevant Federal, State, and Tribal laws, regulations, and other such
mechanisms that may minimize any of the threats we describe in the
threats analysis under the other four factors, or otherwise influence
conservation of the species. We give strongest weight to statutes and
their implementing regulations, and management direction that stems
from those laws and regulations. They are nondiscretionary and
enforceable, and are considered a regulatory mechanism under this
analysis. Having evaluated the significance of the threat as mitigated
by any such conservation efforts, we analyze under Factor D the extent
to which existing regulatory mechanisms are inadequate to address the
specific threats to the species. Regulatory mechanisms, if they exist,
may reduce or eliminate the impacts from one or more identified
threats. In this section, we review existing State and Federal
regulatory mechanisms to determine whether they effectively reduce or
remove threats to the species.
A number of Federal statutes potentially afford protection to
northern Mexican and narrow-headed gartersnakes or their prey species.
These include section 404 of the Clean Water Act (33 U.S.C. 1251 et
seq.), Federal Land Policy and Management Act (43 U.S.C. 1701 et seq.),
National Forest Management Act (16 U.S.C. 1600 et seq.), National
Environmental Policy Act (NEPA; 42 U.S.C. 4321 et seq.), and the Act.
However, in practice, these statutes have not been able to provide
sufficient protection to prevent the currently observed downward trend
in northern Mexican and narrow-headed gartersnakes or their prey
species, and the concurrent upward trend in threats.
Section 404 of the Clean Water Act regulates placement of fill into
waters of the United States, including the majority of northern Mexican
and narrow-headed gartersnake habitat. However, many actions with the
potential to be highly detrimental to both species, their prey base,
and their habitat, such as gravel mining and irrigation diversion
structure construction and maintenance, may be exempted from the Clean
Water Act. Other detrimental actions, such as bank stabilization and
road crossings, are covered under nationwide permits that receive
limited environmental review. A lack of thorough, site-specific
analyses for projects can allow substantial adverse effects to northern
Mexican or narrow-headed gartersnakes, their prey base, or their
habitat.
The majority of the extant populations of northern Mexican and
narrow-headed gartersnakes in the United States occur on lands managed
by the U.S. Bureau of Land Management (BLM) and U.S. Forest Service.
Both agencies have riparian protection goals that may provide habitat
benefits to both species; however, neither agency has specific
management plans for northern Mexican or narrow-headed gartersnakes. As
a result, some of the significant threats to these gartersnakes, for
example, those related to nonnative species, are not addressed on these
lands. The BLM considers the northern Mexican gartersnake as a
``Special Status Species,'' and agency biologists actively attempt to
identify gartersnakes observed incidentally during fieldwork for their
records (Young 2005). Otherwise, no specific protection or land-
management consideration is afforded to that species on BLM lands.
The U.S. Forest Service does not include northern Mexican or
narrow-headed gartersnakes on their Management Indicator Species List,
but both species are included on the Regional Forester's Sensitive
Species List (USFS 2007, pp. 38-39). This means they are considered in
land management decisions, but no specific protective measures are
conveyed to these species. Individual U.S. Forest Service biologists
who work within the range of either northern Mexican or narrow-headed
gartersnakes may opportunistically gather data for their records on
gartersnakes observed incidentally in the field, although it is not
required. The Gila National Forest mentions the narrow-headed
gartersnake in their land and resource management plan, which includes
standards relating to forest management for the benefit of endangered
and threatened species as identified through approved management and
recovery plans (CBD et al. 2011, p. 18). Neither species is mentioned
in any other land and resource management plan for the remaining
national forests where they occur (CBD et al. 2011, p. 18).
The New Mexico Department of Game and Fish lists the northern
Mexican gartersnake as State-endangered and the narrow-headed
gartersnake as State-threatened (NMDGF 2006, Appendix H). A species is
State-endangered if it is in jeopardy of extinction or extirpation
within the State; a species is State-threatened if it is likely to
become endangered within the foreseeable future throughout all or a
significant portion of its range in New Mexico (NMDGF 2006, p. 52).
``Take,'' defined as ``to harass, hunt, capture or kill any wildlife or
attempt to do so'' by NMSA 17-2-38.L., is prohibited without a
scientific collecting permit issued by the New Mexico Department of
Game and Fish as per NMSA 17-2-41.C and New Mexico Administrative Code
(NMAC) 19.33.6. However, while the New Mexico Department of Game and
Fish can issue monetary penalties for illegal take of either northern
Mexican gartersnakes or narrow-headed gartersnakes, the same provisions
are not in place for actions that result in loss or modification of
their habitats (NMSA 17-2-41.C and NMAC 19.33.6) (Painter 2005).
Prior to 2005, the Arizona Game and Fish Department allowed for
take of up to four northern Mexican or narrow-headed gartersnakes per
person per year as specified in Commission Order 43. The Arizona Game
and Fish Department defines ``take'' as ``pursuing, shooting, hunting,
fishing, trapping, killing, capturing, snaring, or netting wildlife or
the placing or using any net or other device or trap in a manner that
may result in the capturing or killing of wildlife.'' The Arizona Game
and Fish Department subsequently amended Commission Order 43, effective
January 2005. Take of northern Mexican and narrow-headed gartersnakes
is no longer permitted in Arizona without issuance of a scientific
collecting permit (Ariz. Admin. Code R12-4-401 et seq.), or special
authorization. While the Arizona Game and Fish Department can seek
criminal or civil penalties for illegal take of these species, the same
provisions are not in place for actions that result in destruction or
modification of the gartersnakes' habitat. In addition to making the
necessary regulatory changes to promote the conservation of northern
Mexican and narrow-headed gartersnakes, the
[[Page 41541]]
Arizona Game and Fish Departments' Nongame Branch continues to be a
strong partner in research and survey efforts that further our
understanding of current populations, and assist with conservation
efforts and the establishment of long-term conservation partnerships.
Throughout Mexico, the Mexican gartersnake is listed at the species
level of its taxonomy as ``Amenazadas,'' or Threatened, by the
Secretaria de Medio Ambiente y Recursos Naturales (SEMARNAT) (SEDESOL
2001). Threatened species are ``those species, or populations of the
same, likely to be in danger of disappearing in a short or medium
timeframe, if the factors that negatively impact their viability, cause
the deterioration or modification of their habitat or directly diminish
the size of their populations continue to operate'' (SEDESOL 2001 (NOM-
059-ECOL-2001), p. 4). This designation prohibits taking of the
species, unless specifically permitted, as well as prohibits any
activity that intentionally destroys or adversely modifies its habitat
(SEDESOL 2000 (LGVS) and 2001 (NOM-059-ECOL-2001)). Additionally, in
1988, the Mexican Government passed a regulation that is similar to the
National Environmental Policy Act of the United States. This Mexican
regulation requires an environmental assessment of private or
government actions that may affect wildlife or their habitat (SEDESOL
1988 (LGEEPA)).
The Mexican Federal agency known as the Instituto Nacional de
Ecolog[iacute]a (INE) is responsible for the analysis of the status and
threats that pertain to species that are proposed for listing in the
Norma Oficial Mexicana NOM-059 (the Mexican equivalent to an endangered
and threatened species list), and, if appropriate, the nomination of
species to the list. INE is generally considered the Mexican
counterpart to the United States' Fish and Wildlife Service. INE
developed the Method of Evaluation of the Risk of Extinction of the
Wild Species in Mexico (MER), which unifies the criteria of decisions
on the categories of risk and permits the use of specific information
fundamental to listing decisions. The MER is based on four independent,
quantitative criteria: (1) Size of the distribution of the taxon in
Mexico; (2) state (quality) of the habitat with respect to natural
development of the taxon; (3) intrinsic biological vulnerability of the
taxon; and (4) impacts of human activity on the taxon. INE began to use
the MER in 2006; therefore, all species previously listed in the NOM-
059 were based solely on expert review and opinion in many cases.
Specifically, until 2006, the listing process under INE consisted of a
panel of scientific experts who convened as necessary for the purpose
of defining and assessing the status and threats that affect Mexico's
native species that are considered to be at risk, and applying those
factors to the definitions of the various listing categories. In 1994,
when the Mexican gartersnake was placed on the NOM-059 (SEDESOL 1994
(NOM-059-ECOL-1994), p. 46) as a threatened species, the decision was
made by a panel of scientific experts.
Although the Mexican gartersnake is listed as a threatened species
in Mexico and based on our experience collaborating with Mexico on
transborder conservation efforts, no recovery plan or other
conservation planning occurs because of this status and enforcement of
the regulation protecting the gartersnake is sporadic, depending on
available resources and location. Based upon the best available
scientific and commercial information on the status of the species, and
the historic and continuing threats to its habitat in Mexico, our
analysis concludes that regulatory mechanisms enacted by the Mexican
government to conserve the northern Mexican gartersnake are not
adequate to address threats to the species or its habitat.
In summary, there are a number of existing regulations that
potentially address issues affecting the northern Mexican and narrow-
headed gartersnakes and their habitats. However, existing regulations
within the range of northern Mexican and narrow-headed gartersnakes
typically only address the direct take of individuals without a permit,
and provide little, if any, protection of gartersnake habitat. Arizona
and New Mexico statutes do not provide protection of habitat and
ecosystems. Legislation in Mexico prohibits intentional destruction or
modification of northern Mexican gartersnake habitat, but neither that,
nor prohibitions of take, appear to be adequate to address ongoing
threats.
Current Conservation of Northern Mexican and Narrow-Headed Gartersnakes
Several conservation measures implemented by land and resource
managers, private land owners, and other stakeholders can directly or
indirectly benefit populations of northern Mexican and narrow-headed
gartersnakes. For example, the AGFD's conservation and mitigation
program (implemented under an existing section 7 incidental take
permit) has committed to either stocking (with captive bred stock) or
securing two populations each of northern Mexican and narrow-headed
gartersnakes to help minimize adverse effects to these species from
their sport fish stocking program through 2021 (USFWS 2011, Appendix
C). However, to achieve these goals, challenges must be overcome.
First, captive propagation of both gartersnake species remains
problematic. After approximately 5 years of experimentation with
captive propagation at five institutions, using two colonies of
northern Mexican gartersnakes and three colonies of narrow-headed
gartersnakes, success has been limited (see GCWG 2007, 2008, 2009,
2010). In 2012, approximately 40 northern Mexican gartersnakes were
produced at one institution, and they were subsequently marked and
released along Cienega Creek. These were the first gartersnakes of
either species to be produced under this program, but their current
status in the wild remains unknown. No narrow-headed gartersnakes have
been produced in captivity under this program since its inception.
Secondly, in order to be successful, the process of ``securing'' a
population of either species will likely involve an aggressive
nonnative removal strategy, and will have to account for habitat
connectivity to prevent reinvasion of unwanted species. Therefore,
securing a population of either species may involve removal of harmful
nonnatives from an entire subbasin.
To improve the status of northern Mexican gartersnakes in this
subbasin, the AGFD recently purchased the approximate 200-acre (81-ha)
Horseshoe Ranch along the Agua Fria River located near the Bloody Basin
Road crossing, east of Interstate 17 and southeast of Cordes Junction,
Arizona. The AGFD plans to introduce northern Mexican gartersnakes as
well as lowland leopard frogs and native fish species into a large
pond, protected by bullfrog exclusion fencing, located adjacent to the
Agua Fria River. The bullfrog exclusion fencing around the pond will
permit the dispersal of northern Mexican gartersnakes and lowland
leopard frogs from the pond, allowing the pond to act as a source
population to the Agua Fria River. The AGFD's short- to mid-term
conservation planning for Horseshoe Ranch will help ensure the northern
Mexican gartersnake persists in this historical stronghold.
In 2007, the New Mexico Department of Game and Fish completed a
recovery plan for narrow-headed gartersnakes in New Mexico (Pierce
2007, pp. 13-15) that included the following management objectives: (1)
Researching the effect of known threats to, and natural history of,
[[Page 41542]]
the species; (2) acquiring funding sources for research, monitoring,
and management; (3) enhancing education and outreach; and (4) managing
against known threats to the species. Implementation of the recovery
plan was to occur between the second half of 2007 through 2011, and was
divided into three main categories: (1) Improve and maintain knowledge
of potential threats to the narrow-headed gartersnake; (2) improve and
maintain knowledge of the biology of the narrow-headed gartersnake; and
(3) develop and maintain high levels of cooperation and coordination
between stakeholders and interested parties (Pierce 2007, pp. 16-17).
Our review of the plan found that it lacked specific threat-mitigation
commitments on the landscape, as well as stakeholder accountability for
implementing activities prescribed in the plan. We also found that
actions calling for targeted nonnative species removal or management
were absent in the implementation schedule provided in Pierce (2007; p.
17). As we have discussed at length, harmful nonnative species are the
primary driver of continued declines in both gartersnake species. No
recovery plan, conservation plan, or conservation agreement currently
exists in New Mexico with regard to the northern Mexican gartersnake
(NMDGF 2006, Table 6-3).
Both northern Mexican and narrow-headed gartersnakes are considered
``Candidate Species'' in the Arizona Game and Fish Department draft
document, Wildlife of Special Concern (WSCA) (AGFD In Prep., p. 12). A
``Candidate Species'' is one ``whose threats are known or suspected but
for which substantial population declines from historical levels have
not been documented (though they appear to have occurred)'' (AGFD In
Prep., p. 12). The purpose of the WSCA list is to provide guidance in
habitat management implemented by land-management agencies.
Additionally, both northern Mexican and narrow-headed gartersnakes are
considered a ``Tier 1b Species of Greatest Conservation Need (SGCN)''
in the Arizona Game and Fish Department document, Arizona's
Comprehensive Wildlife Conservation Strategy (CWCS) (AGFD 2006a, pp.
499-501). The purpose for the CWCS is to ``provide an essential
foundation for the future of wildlife conservation and a stimulus to
engage the States, federal agencies, and other conservation partners to
strategically think about their individual and coordinated roles in
prioritizing conservation efforts'' (AGFD 2006a, p. 2). A ``Tier 1b
SGCN'' is one that requires immediate conservation actions aimed at
improving conditions through intervention at the population or habitat
level (AGFD 2006a, p. 32). In the 2011 draft revised State wildlife
action plan (an updated version of the CWCS), northern Mexican
gartersnake is a Tier 1a SGCN. Tier 1a species ``comprise a large
percentage of [AGFD's] management resource allocation'' and ``are
[their] highest priorities.'' Neither the WSCA nor the CWCS are
regulatory documents and, consequently, do not provide and specific
protections for either the gartersnakes themselves, or their habitats.
The Arizona Game and Fish Department does not have specified or
mandated recovery goals for either the northern Mexican or narrow-
headed gartersnake, nor has a conservation agreement or recovery plan
been developed for either species.
Indirect benefits for both gartersnake species occur through
recovery actions designed for their prey species. Since the Chiricahua
leopard frog was listed as threatened under the Act, significant
strides have been made in its recovery, and the mitigation of its known
threats. The northern Mexican gartersnake, in particular, has likely
benefitted from these actions, at least in some areas, such as at the
Las Cienegas Natural Conservation Area and in Scotia Canyon of the
Huachuca Mountains. However, much of the recovery of the Chiricahua
leopard frog has occurred in areas that have not directly benefitted
the northern Mexican gartersnake, either because these activities have
occurred outside the known distribution of the northern Mexican
gartersnake or because they have occurred in isolated lentic systems
that are far removed from large perennial streams that typically
provide source populations of northern Mexican gartersnakes. In recent
years, significant strides have been made in controlling bullfrogs on
local landscape levels in Arizona, such as in the Scotia Canyon area,
in the Las Cienegas National Conservation Area, on the BANWR, and in
the vicinity of Pena Blanca Lake in the Pajarito Mountains. Recent
efforts to return the Las Cienegas National Conservation Area to a
wholly native biological community have involved bullfrog eradication
efforts, as well as efforts to recover the Chiricahua leopard frog and
native fish species. These actions should assist in conserving the
northern Mexican gartersnake population in this area. Bullfrog control
has been shown to be most effective in simple, lentic systems such as
stock tanks. Therefore, we encourage livestock managers to work with
resource managers in the systematic eradication of bullfrogs from stock
tanks where they occur, or at a minimum, ensure they are never
introduced.
An emphasis on native fish recovery in fisheries management and
enhanced nonnative species control to favor native communities may be
the single most efficient and effective manner to recover these
gartersnakes, in addition to all listed or sensitive native fish and
amphibian species which they prey upon. Alternatively, resource
management policies that either directly benefit or maintain nonnative
community assemblages to the exclusion of native species are likely to
significantly reduce the potential for the conservation and recovery of
northern Mexican and narrow-headed gartersnakes.
Fisheries managers strive to balance the needs of the recreational
angling community against those required by native aquatic communities.
Fisheries management has direct implications for the conservation and
recovery of northern Mexican and narrow-headed gartersnakes in the
United States. Clarkson et al. (2005) discuss management conflicts as a
primary factor in the decline of native fish species in the
southwestern United States, and declare the entire native fish fauna as
imperiled. The investigators cite nonnative species as the most
consequential factor leading to rangewide declines of native fish, and
that such declines prevent or negate species' recovery efforts from
being implemented or being successful (Clarkson et al. 2005, p. 20).
Maintaining the status quo of current management of fisheries within
the southwestern United States will have serious adverse effects to
native fish species (Clarkson et al. 2005, p. 25), which will affect
the long-term viability of northern Mexican and narrow-headed
gartersnakes and their potential for recovery. Clarkson et al. (2005,
p. 20) also note that over 50 nonnative species have been introduced
into the Southwest as either sportfish or baitfish, and some are still
being actively stocked, managed for, and promoted by both Federal and
State agencies as nonnative recreational fisheries.
To help resolve the fundamental conflict of management between
native fish and recreational sport fisheries, Clarkson et al. (2005,
pp. 22-25) propose the designation of entire subbasins as having either
native or nonnative fisheries and manage for these goals aggressively.
The idea of watershed-segregated fisheries management is also supported
by Marsh and Pacey (2005, p. 62). As part of the Arizona Game and Fish
Department's
[[Page 41543]]
overall wildlife conservation strategy, the AGFD has planned an
integrated fisheries management approach (AGFD 2006a, p. 349), which is
apparently designed to manage subbasins specifically for either
nonnative or native fish communities. The AGFD has not yet decided how
fisheries will be managed in Arizona's subbasins. However, angler
access, existing fish communities, and stream flow considerations are
likely to inform such broadly based decisions. Several of Arizona's
large perennial rivers present an array of existing sport fishing
opportunities and access points, contain harmful nonnative fish
species, and also serve as important habitat for either northern
Mexican or narrow-headed gartersnakes. These rivers may be targeted
though this planning exercise for nonnative fisheries management, which
would likely remove any recovery potential for gartersnakes in these
areas, and, perhaps, even result in the local extirpations of
populations of northern Mexican and narrow-headed gartersnakes.
Alternatively, subbasins that are targeted for wholly native species
assemblages would likely secure the persistence of northern Mexican and
narrow-headed gartersnakes that occur there, if not result in their
complete recovery in these areas. Specific subbasins where targeted
fisheries management is to occur were not provided in AGFD (2006a), but
depending on which areas are chosen for each management emphasis, the
potential for future conservation and recovery of northern Mexican and
narrow-headed gartersnakes could either be significantly bolstered, or
significantly hampered. Close coordination with the Arizona Game and
Fish Department on the delineation of fisheries management priorities
in Arizona's subbasins will be instrumental to ensuring that
conservation and recovery of northern Mexican and narrow-headed
gartersnakes can occur.
Conservation of these gartersnakes has been implemented in the
scientific and management communities as well. The AGFD recently
produced identification cards for distribution that provide information
to assist field professionals with the identification of each of
Arizona's five native gartersnake species, as well as guidance on
submitting photographic vouchers for university museum collections.
Arizona State University and the University of Arizona now accept
photographic vouchers in lieu of physical specimens, in their
respective museum collections. These measures appreciably reduce the
necessity for physical specimens (unless discovered postmortem) for
locality voucher purposes and, therefore, further reduce impacts to
vulnerable populations of northern Mexican or narrow-headed
gartersnakes.
Despite these collective efforts we have described above, northern
Mexican and narrow-headed gartersnakes have continued to decline
throughout their ranges.
Proposed Determination
In our review of the best available science, we found that aquatic
ecosystems which northern Mexican and narrow-headed gartersnakes rely
on and are part of have been significantly compromised by harmful
nonnative species. We found this threat to be the most significant and
pervasive of all threats affecting both species. Harmful nonnative
species have been intentionally released or have naturally moved into
virtually every subbasin throughout the range of the northern Mexican
and narrow-headed gartersnakes. This has resulted in widespread
declines in native fish and amphibian communities, which are integral
to the continued survival of the northern Mexican and narrow-headed
gartersnakes. In addition to widespread competitive pressures, harmful
nonnative species have directly impacted both gartersnake species
through predation. In combination, these factors have resulted in
widespread population declines and extirpations in both species, as
neither gartersnake nor their prey evolved in their presence.
In addition to the declining status of the biotic communities where
the northern Mexican and narrow-headed gartersnakes occur, land use
activities, drought, and wildfires threaten vital elements of their
habitat that are important for their survival. Dams, diversions, flood-
control projects, and groundwater pumping have dewatered entire reaches
of historically occupied habitat for both species, rangewide. Large
dams planned in the future threaten to dewater additional reaches.
Climate change predictions include increased aridity, lower annual
precipitation totals, lower snow pack levels, higher variability in
flows (lower low-flows and higher high-flows), and enhanced stress on
ponderosa pine communities in the southwestern United States and
northern Mexico. Increasing water demands from a rapidly growing human
population in the arid southwestern United States, combined with a
drought-limited supply of surface water, fuels future needs for even
more dams, diversions, and groundwater pumping. Due in part to the fire
management policies of recent decades, wildfires in the arid
southwestern United States have grown more frequent and severe. Since
2011, both Arizona and New Mexico experienced the largest wildfires in
their respective State histories. High-intensity wildfires that affect
large areas contribute to significant flooding and sedimentation,
resulting in fish kills and the filling-in of important pool habitat.
These conditions remove a portion of, or the entire prey base, for
northern Mexican and narrow-headed gartersnakes for extended periods of
time. This scenario places significant stress on resident gartersnake
populations through starvation.
Other activities, factors, or conditions that act in combination,
such as mismanaged or unmanaged livestock grazing; road construction,
use, and management; adverse human interactions; environmental
contaminants; erosion control techniques; and competitive pressures
from sympatric species, occur within the distribution of these
gartersnakes and have the tendency to contribute to further population
declines or extirpations where gartersnakes occur at low population
densities. In the presence of harmful nonnative species, the negative
effects of these threats on northern Mexican and narrow-headed
gartersnakes are amplified. Yet, there are currently no regulatory
mechanisms in place to address the threats to these species that
specifically target the conservation of northern Mexican or narrow-
headed gartersnakes or their habitat in the United States or Mexico.
Collectively, the ubiquitous nature of these threats across the
landscape has appreciably reduced the quality and quantity of suitable
gartersnake habitat and changed its spatial orientation on the
landscape. This ultimately renders populations much less resilient to
stochastic, natural, or anthropogenic stressors that could otherwise be
withstood. Over time and space, subsequent population declines have
threatened the genetic representation of each species because many
populations have become disconnected and isolated from neighboring
populations. Expanding distances between extant populations coupled
with threats that prevent normal recolonizing mechanisms leave existing
populations vulnerable to extirpation. This subsequently leads to a
reduction in species redundancy when isolated, small populations are at
increased vulnerability to the effects of stochastic events, without a
means for natural recolonization. Ultimately, the effect of
[[Page 41544]]
scattered, small, and disjunct populations, without the means to
naturally recolonize, is weakened species resiliency as a whole, which
ultimately enhances the risk of the species becoming endangered.
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 have carefully assessed the best
scientific and commercial information available regarding the past,
present, and future threats to the species, and have determined that
the northern Mexican gartersnake and narrow-headed gartersnake both
meet the definition of a threatened species under the Act. Significant
threats are occurring now and are likely to continue in the foreseeable
future, at a high intensity, and across these species' entire ranges;
therefore, we have determined these species are likely to become
endangered throughout all or a significant portion of their ranges
within the foreseeable future. Because these threats are likely to
cause these gartersnakes to become endangered throughout all or a
significant portion of their ranges within the foreseeable future, we
find these species are threatened, not endangered. Therefore, on the
basis of the best available scientific and commercial information, we
propose listing the northern Mexican gartersnake and narrow-headed
gartersnake as threatened species in accordance with sections 3(20) and
4(a)(1) of the Act. The current status of the northern Mexican and
narrow-headed gartersnakes meets the definition of threatened, not
endangered, because while we found numerous threats to be significant
and rangewide, our available survey data conclude that the remaining
small number of populations are viable. Alternatively and based upon
the data available, the northern Mexican and narrow-headed gartersnakes
appear to remain extant, as low-density populations with the threat of
extirpation, in most subbasins where they historically occurred.
Special Rule for Northern Mexican Gartersnake Under Section 4(d) of the
Act
Whenever a species is listed as a threatened species under the Act,
the Secretary may specify regulations that she deems necessary and
advisable to provide for the conservation of that species under the
authorization of section 4(d) of the Act. These rules, commonly
referred to as ``special rules,'' are found in part 17 of title 50 of
the Code of Federal Regulations (CFR) in Sec. Sec. 17.40-17.48. This
proposed special rule for Sec. 17.42 would exempt take of northern
Mexican gartersnakes as a result of livestock use at or maintenance
activities of livestock tanks located on private, State, or Tribal
lands.
The proposed special rule would replace the Act's general
prohibitions against take of the northern Mexican gartersnake with
special measures tailored to the conservation of the species on all
non-Federal lands. Through the maintenance and operation of the stock
tanks for cattle, habitat is provided for the northern Mexican
gartersnake and numerous prey species; hence there is a conservation
benefit to the species. Under the proposed special rule, take of
northern Mexican gartersnake caused by livestock use of or maintenance
activities at livestock tanks located on private, State, or Tribal
lands would be exempt from section 9 of the Act. A livestock tank is
defined as an existing or future impoundment in an ephemeral drainage
or upland site constructed primarily as a watering site for livestock.
The proposed special rule targets tanks on private, State, and Tribal
lands to encourage landowners and ranchers to continue to maintain
these tanks as they provide habitat for the northern Mexican
gartersnake. Livestock use and maintenance of tanks on Federal lands
would be addressed through the section 7 process. When a Federal
action, such as permitting livestock grazing on Federal lands, may
affect a listed species, consultation between us and the action agency
is required under section 7 of the Act. The conclusion of consultation
may include mandatory changes in livestock programs in the form of
measures to minimize take of a listed animal or to avoid jeopardizing
the continued existence of a listed species. Changes in a proposed
action resulting from consultations are almost always minor.
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, preparation of a draft and final
recovery plan, and revisions to the plan as significant new information
becomes available. The recovery outline guides the immediate
implementation of urgent recovery actions and describes the process to
be used to develop a recovery plan. The recovery plan identifies site-
specific management actions that will achieve recovery of the species,
measurable criteria that determine when a species 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 (comprised of species experts, Federal and State
agencies, nongovernment organizations, and stakeholders) are often
established to develop recovery plans. When completed, the recovery
outline, draft recovery plan, and the final recovery plan will be
available on our Web site (http://www.fws.gov/endangered), or from our
Arizona Ecological Services Field Office (see FOR FURTHER INFORMATION
CONTACT).
Implementation of recovery actions generally requires the
participation of a broad range of partners, including other Federal
agencies, States, Tribal, 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 range may occur primarily
[[Page 41545]]
or solely on non-Federal lands. To achieve recovery of these species
requires cooperative conservation efforts on private, State, and Tribal
lands.
If these species are 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,
under section 6 of the Act, the States of Arizona and New Mexico would
be eligible for Federal funds to implement management actions that
promote the protection and recovery of the northern Mexican and narrow-
headed gartersnakes. Information on our grant programs that are
available to aid species recovery can be found at: http://www.fws.gov/grants.
Although the northern Mexican and narrow-headed gartersnakes are
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 these 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
endangered or threatened 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 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' habitats that may
require conference or consultation or both as described in the
preceding paragraph include management and any other landscape altering
activities on Federal lands administered by the Fish and Wildlife
Service, U.S. Bureau of Reclamation, or U.S. Forest Service; issuance
of section 404 Clean Water Act permits by the U.S. Army Corps of
Engineers; construction and management of gas pipeline and power line
rights-of-way by the Federal Energy Regulatory Commission; construction
and maintenance of roads or highways by the Federal Highway
Administration; and other discretionary actions that effect the species
composition of biotic communities where these species or their habitats
occur, such as funding or permitting programs that result in the
continued stocking of nonnative, spiny-rayed fish.
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. The prohibitions
of section 9(a)(2) of the Act, codified at CFR 17.31 for threatened
wildlife, make it such that all the provisions of 50 CFR 17.21 apply,
except Sec. 17.21(c)(5).
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. 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.
It is our policy, as published in the Federal Register on July 1,
1994 (59 FR 34272), 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 effect of a proposed
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) The unauthorized introduction of harmful nonnative species that
compete with or prey upon northern Mexican and narrow-headed
gartersnakes, such as the stocking of nonnative, spiny-rayed fish, or
illegal transport, use, or release of bullfrogs or crayfish in the
States of Arizona and New Mexico;
(3) The unauthorized release of biological control agents that
attack any age class of northern Mexican and narrow-headed gartersnakes
or any life stage of their prey species;
(4) Unauthorized modification of the channel, reduction or
elimination of water flow of any stream or water body, or the complete
removal or significant destruction of riparian vegetation associated
with occupied northern Mexican or narrow-headed gartersnake habitat;
and
(5) Unauthorized discharge of chemicals or fill material into any
waters in which northern Mexican and narrow-headed gartersnakes are
known to occur.
Questions regarding whether specific activities would constitute a
violation of section 9 of the Act should be directed to the Arizona
Ecological Services Field 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, P.O.
Box 1306, Albuquerque, New Mexico 87103 (telephone (505) 248-6920,
facsimile (505) 248-6922).
Peer Review
In accordance with our joint policy on peer review published in the
Federal Register on July 1, 1994 (59 FR 34270), we will seek the expert
opinions of at least three appropriate and independent specialists
regarding this proposed rule. The purpose of peer review is to ensure
that our listing determination is based on scientifically sound data,
assumptions, and analyses. We have invited these peer reviewers to
comment during this public comment period on our specific assumptions
and conclusions in this proposed listing determination.
[[Page 41546]]
We will consider all comments and information received during this
comment period on this proposed rule during our preparation of a final
determination. Accordingly, the final decision may differ from this
proposal.
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.
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 (NEPA; 42 U.S.C. 4321 et seq.), 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 49244).
References Cited
A complete list of references cited in this rulemaking is available
on the Internet at http://www.regulations.gov and upon request from the
Arizona Ecological Services Field Office (see FOR FURTHER INFORMATION
CONTACT).
Authors
The primary authors of this proposed rule are the staff members of
the Arizona Ecological Services Field Office.
List of Subjects in 50 CFR Part 17
Endangered and threatened species, Exports, Imports, Reporting and
recordkeeping requirements, 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:
PART 17--[AMENDED]
0
1. The authority citation for part 17 continues to read as follows:
Authority: 16 U.S.C. 1361-1407; 1531-1544; and 4201-4245,
unless otherwise noted.
0
2. In Sec. 17.11(h), add entries for ``Gartersnake, northern Mexican''
and ``Gartersnake, narrow-headed'' to the List of Endangered and
Threatened Wildlife in alphabetical order under REPTILES to read as
follows:
Sec. 17.11 Endangered and threatened wildlife.
* * * * *
(h) * * *
--------------------------------------------------------------------------------------------------------------------------------------------------------
Species Vertebrate
-------------------------------------------------------- population where Critical Special
Historic range endangered or Status When listed habitat rules
Common name Scientific name threatened
--------------------------------------------------------------------------------------------------------------------------------------------------------
* * * * * * *
REPTILES
* * * * * * *
Gartersnake, northern Mexican.... Thamnophis eques U.S.A. (AZ, NM), Entire............. T............. ........... 17.95(d) 17.42(g)
megalops. Mexico.
* * * * * * *
Gartersnake, narrow-headed....... Thamnophis U.S.A. (AZ, NM).... Entire............. T............. ........... 17.95(d) NA
rufipunctatus.
* * * * * * *
--------------------------------------------------------------------------------------------------------------------------------------------------------
0
3. Amend Sec. 17.42 by adding a new paragraph (g) to read as follows:
Sec. 17.42 Special rules--reptiles.
* * * * *
(g) Northern Mexican gartersnake (Thamnophis eques megalops)--(1)
Which populations of the northern Mexican gartersnake are covered by
this special rule? This rule covers the distribution of this species in
the contiguous United States.
(2) What activities are prohibited? Any activity where northern
Mexican gartersnakes are attempted to be, or are intended to be,
trapped, hunted, shot, or collected, in the contiguous United States,
is prohibited. It is also prohibited to incidentally trap, shoot,
capture, pursue, or collect northern Mexican gartersnakes in the course
of otherwise legal activities.
(3) What activities are allowed? Incidental take of northern
Mexican gartersnakes is not a violation of section 9 of the Act if it
occurs from any other otherwise legal activities involving northern
Mexican gartersnakes and their habitat that are conducted in accordance
with applicable State, Federal, tribal, and local laws and regulations.
Such activities occurring in northern Mexican gartersnake habitat
include maintenance
[[Page 41547]]
activities at livestock tanks located on private, State, or Tribal
lands. A livestock tank is an existing or future impoundment in an
ephemeral drainage or upland site constructed primarily as a watering
site for livestock.
* * * * *
Dated: June 24, 2013.
Daniel M. Ashe,
Director, U.S. Fish and Wildlife Service.
[FR Doc. 2013-16521 Filed 7-9-13; 8:45 am]
BILLING CODE 4310-55-P