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Endangered and Threatened Wildlife and Plants; 12-Month Finding on a Petition To List the Northern Mexican Gartersnake (Thamnophis eques megalops) as Threatened or Endangered With Critical Habitat
Note: EPA no longer updates this information, but it may be useful as a reference or resource.
[Federal Register: September 26, 2006 (Volume 71, Number 186)]
[Proposed Rules]
[Page 56227-56256]
From the Federal Register Online via GPO Access [wais.access.gpo.gov]
[DOCID:fr26se06-26]
[[Page 56228]]
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DEPARTMENT OF THE INTERIOR
Fish and Wildlife Service
50 CFR Part 17
Endangered and Threatened Wildlife and Plants; 12-Month Finding
on a Petition To List the Northern Mexican Gartersnake (Thamnophis
eques megalops) as Threatened or Endangered With Critical Habitat
AGENCY: Fish and Wildlife Service, Interior.
ACTION: Notice of 12-month petition finding.
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SUMMARY: We, the U.S. Fish and Wildlife Service (Service), announce a
12-month finding on a petition to list the northern Mexican gartersnake
(Thamnophis eques megalops) as threatened or endangered with critical
habitat under the Endangered Species Act of 1973, as amended (Act). The
petitioners provided three listing scenarios for consideration by the
Service: (1) Listing the United States population as a Distinct
Population Segment (DPS); (2) listing Thamnophis eques megalops
throughout its range in the United States and Mexico based on its
rangewide status; or (3) listing Thamnophis eques megalops throughout
its range in the United States and Mexico based on its status in the
United States. After thorough analysis and review of all available
scientific and commercial information, we find that listing of the
subspecies, under any of the three scenarios, is not warranted. Of the
three listing scenarios specified above, we found scenario two provided
the most rigorous evaluation of the status of the northern Mexican
gartersnake and herein provide detailed discussion of our conclusions
in that context. We also provide additional discussion of our
evaluation of scenarios (1) listing the United States population as a
DPS and (3) listing Thamnophis eques megalops throughout its range in
the United States and Mexico based on its status in the United States.
DATES: The finding announced in this document was made on September 26,
2006.
ADDRESSES: The complete supporting file for this finding is available
for inspection, by appointment, during normal business hours at the
Arizona Ecological Services Office, 2321 West Royal Palm Road, Suite
103, Phoenix, AZ 85021-4951. Please submit any new information,
materials, comments, or questions concerning this species or this
finding to the above address.
FOR FURTHER INFORMATION CONTACT: Steve Spangle, Field Supervisor,
Arizona Ecological Services Office (see ADDRESSES) 602-242-0210.
SUPPLEMENTARY INFORMATION:
Background
Section 4(b)(3)(B) of the Act (16 U.S.C. 1531 et seq.), requires
that, for any petition to revise the Lists of Threatened and Endangered
Wildlife and Plants that contains substantial scientific and commercial
information that listing may be warranted, we make a finding within 12
months of the date of receipt of the petition on whether the petitioned
action is (a) not warranted, (b) warranted, or (c) warranted, but that
the immediate proposal of a regulation implementing the petitioned
action is precluded by other pending proposals to determine whether any
species is threatened or endangered, and expeditious progress is being
made to add or remove qualified species from the Lists of Endangered
and Threatened Wildlife and Plants. Section 4(b)(3)(C) of the Act
requires that a petition for which the requested action is found to be
warranted but precluded be treated as though resubmitted on the date of
such finding, i.e., requiring a subsequent finding to be made within 12
months. Each subsequent 12-month finding will be published in the
Federal Register.
On December 19, 2003, we received a petition 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, submitted by the Center
for Biological Diversity, 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 Mr.
Noah Greenwald, dated March 1, 2004. In that letter, we also advised
the petitioners 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 petitioners filed a complaint for declaratory
and injunctive relief, challenging our failure to issue a 90-day
finding 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 positive, 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 (Thamnophis eques megalops) may be
warranted, but we did not discuss the applicability of any of the three
listing scenarios that were provided in the petition. The finding and
our initiation of a status review was published in the Federal Register
on January 4, 2006 (71 FR 315). We are required, under the court-
approved stipulated settlement agreement, to submit to the Federal
Register our 12-month finding pursuant to the Act [16 U.S.C.
1533(b)(3)(B)]
on or before September 15, 2006. This notice constitutes
our 12-month finding for the petition to list the northern Mexican
gartersnake as threatened or endangered.
Previous Federal Actions
The Mexican gartersnake (Thamnophis eques) (which included the
subspecies) was placed on the list of candidate species as a Category 2
species in 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 gartersnake was no longer
recognized as a candidate. In addition, on January 4, 2006, we
published a 90-day finding on a petition to list the northern Mexican
gartersnake (71 FR 315), as discussed above.
Biology
Species Description. The northern Mexican gartersnake may occur
with other native gartersnake species and can be difficult for people
without herpetological expertise to identify. With a maximum known
length of 44 inches (in) (112 centimeters (cm)), it ranges in
background color from olive to olive-brown to olive-gray with three
stripes that run the length of the body. The middle dorsal stripe is
yellow and darkens toward the tail. The pale yellow to light-tan
lateral stripes distinguish the Mexican gartersnake from other sympatric
(co-occurring) gartersnake species because a portion of the lateral
[[Page 56229]]
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 and the olive-gray ventrolateral fields. A
conspicuous, light-colored crescent extends behind the corners of the
mouth. The two dark brown to black blotches that occur behind the head
of several gartersnake species may be diffuse or absent in the Mexican
gartersnake. The coloration of the venter is bluish-gray or greenish-
grey. The dorsolateral scalation is keeled, the anal plate is single,
and there are eight or nine upper labial scales (Rosen and Schwalbe
1988, p. 4; Rossman et al. 1996, pp. 171-172).
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 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).
There are approximately 30 species that have been described in the
gartersnake genus Thamnophis (Rossman et al. 1996, p. xvii-xviii). De
Queiroz et al. (2002, p. 323) identified two large overlapping clades
(related taxonomic groups) of gartersnakes that they called the
``Mexican'' and ``widespread'' clades which were supported by allozyme
and mitochondrial DNA genetic analyses. Thamnophis eques is a member of
the ``widespread'' clade and is most closely related taxonomically to,
although genetically and phenotypically distinct from, the checkered
gartersnake (Thamnophis marcianus) (De Queiroz and Lawson 1994, p. 217).
Rossman et al. (1996, p. 175) noted that the current specific name
eques was not applied at the time of the original description of the
holotype because the specimen was mistakenly identified as a black-
necked gartersnake (Thamnophis cyrtopsis). In recent history and 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). T. eques displays considerable phenotypic variability
(variation in its physical appearance) across its distribution, and all
subspecific descriptions under T. eques have been based on
morphometrics or morphological characters. The subspecies T. e. eques
and T. e. megalops are distinguished by average differences in sub-
caudal scale counts, while T. e. virgatenuis is distinguished from T.
e. megalops based on having a darker background color and a narrower
vertebral stripe (Rossman et al. 1996, p. 175). Rossman et al. (1996,
p. 175) also noted that the discontinuous distributions of high-
elevation and low-elevation T. e. virgatenuis and T. e. megalops,
respectively, are ``zoogeographically peculiar and unique among
gartersnakes.''
Rossman et al. (1996, p. 172) describe the distribution of T. e.
eques as occurring from southern Nayarit eastward along the Transverse
Volcanic Axis to west-central Veracruz, and identified an additional
disjunct population in central Oaxaca. T. e. virgatenuis is distributed
in three isolated, high-elevation populations in southwestern Durango
and in west-central and northwestern Chihuahua (Rossman et al. 1996, p.
172).
In 2003, an additional seven new subspecies were identified under
T. eques: (1) T. e. cuitzeoensis; (2) T. e. patzcuaroensis; (3) T. e.
inspiratus; (4) T. e. obscurus; (5) T. e. diluvialis; (6) T. e.
carmenensis; and (7) T. e. scotti (Conant 2003, p. 3). These seven new
subspecies were described based on morphological differences in
coloration and pattern; have high endemism (degree of restriction to a
particular area) with 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). We are not aware of any challenges
within the scientific literature of the validity of current taxonomy of
any of the 10 subspecies of T. eques.
The most widely distributed of the 10 subspecies under Thamnophis
eques is the northern Mexican gartersnake (Thamnophis eques megalops),
which is the only subspecies that occurs in the United States and the
entity we address in this finding. In Mexico, T. e. megalops
historically occurred throughout the Sierra Madre Occidental south to
Guanajuato, and east across the Mexican Plateau to Hidalgo, which
comprised approximately 85 percent of the total rangewide distribution
of the species (Rossman et al. 1996, p. 173). Robert Kennicott first
described the northern Mexican gartersnake in 1860, as Eutenia megalops
from the type locality of Tucson, Arizona (Rosen and Schwalbe 1988, p.
2). In 1951, Dr. Hobart Smith renamed the subspecies with its current
scientific name (Rosen and Schwalbe 1988, p. 3). A summary of this
species' lengthy taxonomic history can be found in Rosen and Schwalbe
(1988, pp. 2-3). Several common names have been applied to the northern
Mexican gartersnake in the United States over the years, such as the
Arizona ribbon snake, the Emory's gartersnake, and the Arizona
gartersnake (Rosen and Schwalbe 1988, p. 2).
In summary, while the taxonomic history of Thamnophis eques is
robust, we found no indication in the significant body of taxonomic
literature we reviewed that its current taxonomy is in doubt or in any
way invalid (Rosen and Schwalbe 1988, pp. 2-3; De Queiroz and Lawson
1994, pp. 215-217; Liner 1994, p. 107; Rossman et al. 1996, pp. 171,
175; Conant 2003, p. 6; Crother et al. 2000, p. 72; 2003, p. 202; De
Queiroz et al. 2002, p. 327).
Habitat. 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). The northern
Mexican gartersnake is considered 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), stock tanks (small earthen
impoundment), etc.]; (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; Arizona Game and Fish Department
2001). Vegetation characteristics vary based on the type of habitat.
For example, in source-area wetlands, dense vegetation consists of knot
grass (Paspalum distichum), spikerush (Eleocharis), bulrush (Scirpus),
cattail (Typha), deergrass (Muhlenbergia), sacaton (Sporobolus),
Fremont cottonwood (Populus fremontii), Goodding's willow (Salix
gooddingii), and velvet mesquite (Prosopis velutina) (Rosen and
Schwalbe 1988, pp. 14-16).
In riparian woodlands consisting of cottonwood and willow or
gallery forests of broadleaf and deciduous species along larger rivers,
the northern Mexican gartersnake may be observed in mixed grasses along
the bank or in the shallows (Rossman et al. 1996, p. 176; Rosen and
Schwalbe 1988, p. 16). Within and adjacent to the Sierra Madre
Occidental in Mexico, it occurs in montane woodland, Chihuahuan
desertscrub, mesquite-grassland, and Cordillera Volc[aacute]nica
montane woodland (McCranie and Wilson 1987, pp. 14-17).
[[Page 56230]]
In small streamside riparian habitat, this snake is often
associated with Arizona sycamore (Platanus wrightii), sugar leaf maple
(Acer grandidentatum), velvet ash (Fraxinus velutina), Arizona cypress
(Cupressus arizonica), Arizona walnut (Juglans major), Arizona alder
(Alnus oblongifolia), alligator juniper (Juniperus deppeana), Rocky
Mountain juniper (J. scopulorum), and a number of oak species (Quercus
spp.) (McCranie and Wilson 1987, pp. 11-12; Cirett-Galan 1996, p. 156).
Behavior, Prey Base, and Reproduction. The northern Mexican
gartersnake is surface active at ambient 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. 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).
Generally, its diet consists predominantly of amphibians and fishes,
such as adult and larval native leopard frogs [e.g., lowland leopard
frog (Rana yavapaiensis) and Chiricahua leopard frog (Rana
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).
Auxiliary prey items may also include young Woodhouse's toads (Bufo
woodhousei), treefrogs (Family Hylidae), earthworms, deermice
(Peromyscus maniculatus), lizards of the genera Aspidoscelis and
Sceloporus, larval tiger salamanders (Ambystoma tigrinum), and leeches
(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). To a much lesser extent, this snake's diet may include nonnative
species, including juvenile fish, larval and juvenile bullfrogs, and
mosquitofish (Gambusia affinis) (Holycross et al. 2006, p. 23).
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
ovoviviparous (eggs develop and hatch within the oviduct of the
female). Mating occurs in April and May in their northern distribution
followed by the live birth of between 7 and 26 neonates (newly born
individuals) (average is 13.6) in July and August (Rosen and Schwalbe
1988, p. 16). Approximately half of the sexually mature females within
a population reproduce in any one season (Rosen and Schwalbe 1988, p. 17).
Distribution
Historical Distribution. The United States comprises the northern
portion of the northern Mexican gartersnake's distribution. Within the
United States, the northern Mexican gartersnake historically occurred
predominantly in Arizona with a limited distribution in New Mexico that
consisted of scattered locations throughout the Gila and San Francisco
headwater drainages in western Hidalgo and Grant counties (Price 1980,
p. 39; Fitzgerald 1986, Table 2; Degenhardt et al. 1996, p. 317;
Holycross et al. 2006, pp. 1-2). Fitzgerald (1986, Table 2) provided
museum records for the following historical localities for northern
Mexican gartersnakes in New Mexico: (1) Mule Creek; (2) the Gila River,
5 miles (mi) ( 8 kilometers (km)) east of Virden; (3) Spring Canyon;
(4) the West Fork Gila River at Cliff Dwellings National Monument; (5)
the Tularosa River at its confluence with the San Francisco River; (6)
the San Francisco River at Tub Spring Canyon; (7) Little Creek at
Highway 15; (8) the Middle Box of Gila River at Ira Ridge; (9) Turkey
Creek; (10) Negrito Creek; and (11) the Rio Mimbres.
Within Arizona, the historical distribution of the northern Mexican
gartersnake ranged from 130 to 6,150 ft (40 to 1,875 m) in elevation
and spread variably based on the relative permanency of water and the
presence of suitable habitat. In Arizona, the northern Mexican
gartersnake historically occurred within several perennial or
intermittent drainages and disassociated wetlands that included: (1)
The Gila River; (2) the Lower Colorado River from Davis Dam to the
International Border; (3) the San Pedro River; (4) the Santa Cruz River
downstream from the International Border; (5) the Santa Cruz River
headwaters/San Rafael Valley and adjacent montane canyons; (6) the Salt
River; (7) the Rio San Bernardino from International Border to
headwaters at Astin Spring (San Bernardino National Wildlife Refuge);
(8) Agua Fria River; (9) the Verde River; (10) Tanque Verde Creek in
Tucson; (11) Rillito Creek in Tucson; (12) Agua Caliente Spring in
Tucson; (13) the downstream portion of the Black River from the Paddy
Creek confluence; (14) the downstream portion of the White River from
the confluence of the East and North forks; (15) Tonto Creek from the
mouth of Houston Creek downstream to Roosevelt Lake; (16) Cienega Creek
from the headwaters to the ``Narrows'' just downstream of Apache
Canyon; (17) Pantano Wash (Cienega Creek) from Pantano downstream to
Vail; (18) Potrero Canyon/Springs; (19) Audubon Research Ranch and
vicinity near Elgin; (20) Upper Scotia Canyon in the Huachuca
Mountains; (21) Arivaca Creek; (22) Arivaca Cienega; (23) Sonoita
Creek; (24) Babocomari River; (25) Babocamari Cienega; (26) Barchas
Ranch, Huachuca Mountain bajada; (27) Parker Canyon Lake and
tributaries in the Canelo Hills; (28) Big Bonito Creek; (29) Lake
O'Woods, Lakeside area; (30) Oak Creek from Midgley Bridge downstream
to the confluence with the Verde River; and (31) Spring Creek above the
confluence with Oak Creek (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; Rosen 2006; Holycross 2006).
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 (De Queiroz and Smith 1996, p. 155); however, any
populations of northern Mexican gartersnakes that may have historically
occurred in Nevada pertained directly to the Colorado River and are
likely 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, Coahila, Zacatecas,
Guanajuato, Nayarit, Hidalgo, Jalisco, San Luis Potos[iacute],
Aguascalientes, Tlaxacala, Puebla, M[eacute]xico, Veracruz, and
Quer[eacute]taro, which comprises approximately 70 to 80 percent of its
historical rangewide distribution (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).
Status in the United States. Holycross et al. (2006, p. 12)
included the northern Mexican gartersnake as a target species at 33
sites surveyed within drainages along the Mogollon Rim. A total of 874
person-search hours and 63,495 trap-hours were devoted to that effort,
which resulted in the capture of 23 snakes total in 3 (9 percent) of
the sites visited. This equates to approximately 0.03 snakes observed
per person-search hour and 0.0004 snakes captured per trap-hour over
the entire effort. For comparison, a population of northern Mexican
gartersnakes at Page Springs, Arizona,
[[Page 56231]]
that we consider stable yielded 0.22 snakes observed per person-search
hour and 0.004 snakes captured per trap-hour (an order of magnitude
higher) (Holycross et al. 2006, p. 23). Survey sites were selected
based on the existence of historical records for the species or sites
where the species may occur based on habitat suitability within the
historical distribution of the species. Holycross et al. (2006, p. 12)
calculated the capture rates for the northern Mexican gartersnake as
12,761 trap-hours per snake and 49 person-search hours per snake.
Northern Mexican gartersnakes were found at 2 of 11 (18 percent)
historical sites and 1 of 22 (4 percent) sites where the species was
previously unrecorded (Holycross et al. 2006, p. 12). When compared
with extensive survey data in Rosen and Schwalbe (1988, Appendix I),
these data demonstrate dramatic declines in both capture rates and the
total number of populations of the species in areas where multiple
surveys have been completed over time. However, these data may be
affected by differences in survey efforts and drought.
In 2000, Rosen et al. (2001, Appendix I) resurveyed many sites in
southeastern Arizona that were historically known to support northern
Mexican gartersnake populations during the early to mid-1980s, and also
provided additional survey data collected from 1993-2001. Rosen et al.
(2001, pp. 21-22) reported their results in terms of increasing,
stabilized, or decreasing populations of northern Mexican gartersnakes.
Three sites (San Bernardino National Wildlife Refuge, Finley Tank
at the Audubon Research Ranch near Elgin, and Scotia Canyon in the
Huachuca Mountains) were intensively surveyed and yielded mixed
results. The northern Mexican gartersnake population on the San
Bernardino National Wildlife Refuge experienced ``major, demonstrable
declines'' to near or at extirpation over the span of a decade. That
population is now considered extirpated (Radke 2006). The status of the
population at Finley Tank is uncertain. Scotia Canyon was the last area
intensively resurveyed by Rosen et al. (2001, pp. 15-16). In comparing
this information with survey data from Holm and Lowe (1995, pp. 27-35),
northern Mexican gartersnake populations in this area suggest a
possible decline from the early 1980s, as evidenced by low capture
rates in 1993 and even lower capture rates in 2000.
The remaining 13 sites in southeastern Arizona resurveyed by Rosen
et al. (2001, pp. 21-22) also yielded mixed results. Population trend
information is difficult to ascertain given the variability of survey
sample design and effort used by Rosen et al. (2001). However, the
survey results suggested population increases at one site (lower
Cienega Creek), possible stability at two sites (lower San Rafael
Valley, Arivaca), and negative trends at many other sites [Empire-
Cienega Creek, Babocomari, Bog Hole, O'Donnell Creek, Turkey Creek
(Canelo), Post Canyon, Lewis Springs (San Pedro River), San Pedro River
near Highway 90, Barchas Ranch Pond (Huachuca Mountain bajada), Heron
Spring, Sharp Spring, and Elgin-Sonoita windmill well site (San Rafael
Valley)]
(Rosen et al. 2001, pp. 21-22). While this survey effort could
not confirm any specific extirpations of northern Mexican gartersnake
populations on a local scale in southeastern Arizona, most sites
yielded no snakes during resurvey (Rosen et al. 2001, Appendix I).
Our analysis of the best available data on the status of the
northern Mexican gartersnake distribution in the United States
indicates that its distribution has been significantly reduced in the
United States, and it is now considered extirpated from New Mexico
(Nickerson and Mays 1970, p. 503; Rosen and Schwalbe 1988, pp. 25-26,
Appendix I; Holm and Lowe 1995, pp. 27-35; Sredl et al. 1995b, pp. 2,
9-10; 2000, p. 9; Rosen et al. 2001, Appendix I; Painter 2005, 2006;
Holycross et al. 2006, p. 66; Brennan and Holycross 2006, p. 123; Radke
2006; Rosen 2006; Holycross 2006). Fitzgerald (1986, pp. 9-10) visited
33 localities of potential habitat for northern Mexican gartersnakes in
New Mexico in the Gila River drainage and was unable to confirm its
existence at any of these sites. The New Mexico Department of Game and
Fish State Herpetologist, Charles Painter, provided several causes that
have synergistically contributed to the decline of northern Mexican
gartersnakes in New Mexico, including bullfrog and nonnative fish
introductions, modification and destruction of habitat, commercial
exploitation, direct human-inflicted harm, and fragmentation of
populations. The last known observation of the northern Mexican
gartersnake in New Mexico occurred in 1994 on private land (Painter
2000, p. 36; Painter 2005).
Our analysis of the best available information indicates that the
northern Mexican gartersnake has likely been extirpated from a large
portion of its historical distribution in the United States. We define
a population as ``likely extirpated'' when there have been no northern
Mexican gartersnakes reported for a decade or longer at a site within
the historical distribution of the species, despite at least minimal
survey efforts, and natural recovery at the site is not expected due to
the presence of known threats. The perennial or intermittent stream
reaches and disassociated wetlands where the northern Mexican
gartersnake has likely been extirpated include: (1) The Gila River; (2)
the Lower Colorado River from Davis Dam to the International Border;
(3) the San Pedro River; (4) the Santa Cruz River downstream from the
International Border at Nogales; (5) the Salt River; (6) the Rio San
Bernardino from International Border to headwaters at Astin Spring (San
Bernardino National Wildlife Refuge); (7) the Agua Fria River; (8) the
Verde River upstream of Clarkdale; (9) the Verde River from the
confluence with Fossil Creek downstream to its confluence with the Salt
River; (10) Tanque Verde Creek in Tucson; (11) Rillito Creek in Tucson;
(12) Agua Caliente Spring in Tucson; (13) Potrero Canyon/Springs; (14)
Babocamari Cienega; (15) Barchas Ranch, Huachuca Mountain bajada; (16)
Parker Canyon Lake and tributaries in the Canelo Hills; and (17) Oak
Creek at Midgley Bridge (Rosen and Schwalbe 1988, pp. 25-26, Appendix
I; 1997, pp. 16-17; Rosen et al. 2001, Appendix I; Brennan and
Holycross 2006, p. 123; Holycross 2006; Holycross et al. 2006, pp. 15-
51, 66; Radke 2006; Rosen 2006). Information pertaining to the cause or
causes of extirpation of these sites is summarized in Table 1 below.
Conversely, our review of the best available information indicates
the northern Mexican gartersnake is likely extant in a fraction of its
historical range in Arizona. We define populations as ``likely extant''
when the species is expected to reliably occur in appropriate habitat
as supported by recent museum records and/or recent (i.e., less than 10
years) reliable observations. The perennial or intermittent stream
reaches and disassociated wetlands where we conclude northern Mexican
gartersnakes remain extant include: (1) The Santa Cruz River/Lower San
Rafael Valley (headwaters downstream to the International Border); (2)
the Verde River from the confluence with Fossil Creek upstream to
Clarkdale; (3) Oak Creek at Page Springs; (4) Tonto Creek from the
mouth of Houston Creek downstream to Roosevelt Lake; (5) Cienega Creek
from the headwaters downstream to the ``Narrows'' just downstream of
Apache Canyon; (6) Pantano Wash (Cienega Creek) from Pantano downstream
to Vail; (7) Upper Scotia Canyon in the Huachuca Mountains; and (8) the
Audubon Research Ranch and vicinity near Elgin
[[Page 56232]]
(Rosen et al. 2001, Appendix I; Caldwell 2005; Brennan and Holycross
2006, p. 123; Holycross 2006; Holycross et al. 2006, pp. 15-51, 66;
Rosen 2006).
The current status of the northern Mexican gartersnake is unknown
in several areas in Arizona where the species is known to have
historically occurred. We base this determination on mostly historical
museum records for locations where survey access is restricted, survey
data are unavailable or insufficient, and/or current threats could
preclude occupancy. The perennial or intermittent stream reaches and
disassociated wetlands where the status of the northern Mexican
gartersnake remains uncertain include: (1) The downstream portion of
the Black River drainage from the Paddy Creek confluence; (2) the
downstream portion of the White River drainage from the confluence of
the East and North forks; (3) Big Bonito Creek; (4) Lake O'Woods near
Lakeside; (5) Spring Creek above the confluence with Oak Creek; (6) Bog
Hole Wildlife Area; (7) Upper 13 Tank, Patagonia Mountain bajada; (8)
Babocamari River; and (9) Arivaca Cienega (Rosen and Schwalbe 1988,
Appendix I; Rosen et al. 2001, Appendix I; Brennan and Holycross 2006,
p. 123; Holycross 2006; Holycross et al. 2006, pp. 15-51; Rosen 2006).
In summary, after consultation with species' experts and land
managers, and based upon our analysis of the best available scientific
and commercial data, we conclude that the northern Mexican gartersnake
has been extirpated from 85 to 90 percent of its historical
distribution in the United States.
Status in Mexico. Throughout this finding, and due to the
significantly limited amount of available literature that addresses the
status of and threats to extant populations of the northern Mexican
gartersnake in Mexico, we rely in part on (1) information that
addresses the status of and threats to both riparian and aquatic
biological communities within the historical distribution of the
northern Mexican gartersnake in Mexico; and (2) information that
addresses the status of and threats to native freshwater fish within
the historical distribution of the northern Mexican gartersnake in
Mexico, which we use as ecological surrogates due to their similar
habitat requirements and their role as important prey species utilized
by the northern Mexican gartersnake. Observations on the status of
riparian and aquatic communities in Mexico are available but limited in
comparison to our knowledge of these communities in the United States.
The current distribution of the northern Mexican gartersnake in Mexico
is also not well understood, although its status is believed to be in
decline in many areas due to historical and continuing threats to its
habitat and prey base, as discussed below. A large number of springs
have dried up in several Mexican states within the distribution of the
northern Mexican gartersnake, namely, Chihuahua, Durango, Coahila, and
San Luis Potos[iacute]
(Contreras Balderas and Lozano 1994, p. 381).
Contreras Balderas and Lozano (1994, p. 381) also stated that several
streams and rivers throughout Mexico and within the distribution of the
northern Mexican gartersnake have dried up or become intermittent due
to overuse of surface and groundwater supplies. We further acknowledge
that northern Mexican gartersnakes were historically distributed in
several regions within Mexico that have remained roadless and isolated
and, according to the information we were able to obtain regarding the
status of the northern Mexican gartersnake in Mexico, few ecological
investigations have occurred in these areas due to their remote nature
and the logistical difficulties that face research in such areas.
However, Mexican biologists Ramirez Bautista and Arizmendi (2004, p. 3)
were able to provide general information on the principal threats to
northern Mexican gartersnake habitat in Mexico which included the
dessication of wetlands, improper livestock grazing, deforestation,
wildfires, and urbanization. In addition, nonnative species, such as
bullfrogs and sport and bait 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). Given the lack of specific data on the status of the northern
Mexican gartersnake in Mexico, we cannot conclude with any degree of
certainty its overall status in Mexico.
Northern Mexican Gartersnake Distinct Population Segment
In the petition to list the northern Mexican gartersnake, the
petitioners specified several listing options for our consideration,
including listing northern Mexican gartersnake in the United States as
a DPS. Under the Act, we must consider for listing any species,
subspecies, or DPSs of vertebrate species/subspecies, if information is
sufficient to indicate that such action may be warranted. To implement
the measures prescribed by the Act and its Congressional guidance, we
developed a joint policy with the National Oceanic and Atmospheric
Administration (NOAA) Fisheries entitled Policy Regarding the
Recognition of Distinct Vertebrate Population (DPS Policy) to clarify
our interpretation of the phrase ``distinct population segment of any
species of vertebrate fish or wildlife'' for the purposes of listing,
delisting, and reclassifying species under the Act (61 FR 4721;
February 7, 1996). Under our DPS policy, we consider three elements in
a decision regarding the status of a possible DPS as endangered or
threatened under the Act. The elements are: (1) The population
segment's discreteness from the remainder of the taxon to which it
belongs; (2) the population segment's significance to the taxon to
which it belongs; and (3) the population segment's conservation status
in relation to the Act's standards for listing (i.e., when treated as
if it were a species, is the population segment endangered or
threatened?). Our policy further recognizes it may be appropriate to
assign different classifications (i.e., threatened or endangered) to
different DPSs of the same vertebrate taxon (61 FR 4721; February 7, 1996).
Discreteness
The DPS policy's standard for discreteness requires an entity given
DPS status under the Act to be adequately defined and described in some
way that distinguishes it from other populations of the species. A
population segment may be considered discrete if it satisfies either
one of the following conditions: (1) Marked separation from other
populations of the same taxon resulting from physical, physiological,
ecological, or behavioral factors, including genetic discontinuity; or
(2) populations delimited by international boundaries within which
differences in control of exploitation, management of habitat,
conservation status, or regulatory mechanisms exist that are
significant in light of 4(a)(1)(D) of the Act.
Marked Separation from Other Populations of the Same Taxon as a
Consequence of Physical, Physiological, Ecological or Behavioral
Factors. We do not have any information to indicate that a marked
separation exists between the United States and Mexico that would
distinguish populations of northern Mexican gartersnake in the United
States from those in Mexico. There is no information to indicate that a
marked separation exists as a result of physical, physiological,
ecological, or behavioral factors.
There has been no genetic analysis completed for the northern
Mexican gartersnake. Thus, we have no information to indicate that
genetic differences exist.
[[Page 56233]]
Populations Delimited by International Boundaries Within Which
Differences in Control of Exploitation, Management of Habitat,
Conservation Status, or Regulatory Mechanisms Exist that are
Significant. In terms of the conservation status of the northern
Mexican gartersnake, despite the significantly limited amount of
monitoring and/or survey data for the northern Mexican gartersnake in
Mexico, we believe there is a higher probability that the subspecies is
fairing better overall in Mexico in terms of having more total
populations, because a larger percentage of the overall range of the
subspecies (approximately 70 to 80 percent of it historical
distribution) occurs in Mexico. However, we have no information to
indicate that the populations on either side of the United States-
Mexico border have a more stable or better conservation status.
We recognize that differences in management regulatory protection
of northern Mexican gartersnake populations may exist between
populations within Mexico and those within the United States. These
differences primarily pertain to protections afforded to occupied
habitat. In Mexico, any activity that intentionally destroys or
adversely modifies occupied northern Mexican gartersnake habitat is
prohibited [SEDESOL 2000 (LGVS) and 2001 (NOM-059-ECOL-2001)]. Neither
the Arizona Game and Fish Department or the New Mexico Department of
Game and Fish can offer protections to occupied habitat. Instead, these
agencies regulate take in the form of lethal or live collection of
individuals which is prohibited in both states. However, any
conclusions that may be drawn with reference to differences in
management across the United States-Mexico border are largely
speculative due to the lack of information available as to the efficacy
and protections of these regulations in practice. Because we determine
in the following section that populations of the northern Mexican
gartersnake in the United States are not significant to the subspecies
as a whole, we need not address further the ``discreteness'' test of
the DPS policy. For further information on regulatory considerations,
please see our discussion under Factor D below.
Significance
Under our DPS policy, a population segment must be significant to
the taxon to which it belongs. The evaluation of ``significance'' may
address, but is not limited to, (1) evidence of the persistence of the
discrete population segment in an ecological setting that is unique for
the taxon; (2) evidence that loss of the population segment would
result in a significant gap in the range of the taxon; (3) evidence
that the population segment represents the only surviving natural
occurrence of a taxon that may be more abundant elsewhere as an
introduced population outside its historic range; and (4) evidence that
the discrete population segment differs markedly from other populations
of the species in its genetic characteristics.
Ecological Setting. Throughout its rangewide distribution, the
northern Mexican gartersnake occurs at elevations from 130 to 8,497 ft
(40 to 2,590 m) (Rossman et al. 1996, p. 172). The northern Mexican
gartersnake is considered a riparian obligate (restricted to riparian
areas when not engaged in dispersal behavior) and occurs chiefly in the
following general habitat types in both the United States and Mexico:
(1) Source--area wetlands [e.g., cienegas (mid-elevation wetlands with
highly organic, reducing (basic, or alkaline) soils), stock tanks
(small earthen impoundment), etc.]; (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; Arizona Game and Fish
Department 2001). Based on this information, we determine that
populations of the northern Mexican gartersnake in Arizona do not
occupy an ecological setting differing enough from populations that
occur in Mexico to be considered unique for the subspecies.
Gap in the Range. The Service can determine that a gap in a taxon's
range caused by the potential loss of a population would be significant
based on any relevant considerations. One factor which may support such
a determination is whether the loss of a geographic area amounts to a
substantial reduction of a taxon's range and this reduction is
biologically important. The United States comprised the most northern
portion of the northern Mexican gartersnake's range and constituted
approximately 20-30 percent of its rangewide historical distribution.
Because we do not currently know exactly what the status of the
northern Mexican gartersnake is in Mexico at this time, we are unable
to ascertain what percentage of extant populations occur in the United
States as compared to Mexico. However, this is not sufficient evidence
to support a determination that loss of the northern Mexican
gartersnake in the United States represents a substantial reduction in
the subspecies' range based on the geographic area which would be lost.
Furthermore, no area that is uniquely biologically significant to the
northern Mexican gartersnake is located within the United States as
compared to Mexico.
Another factor relevant to determining whether a gap is significant
is the biological significance of the number of total individuals of
the taxon in the population that may be lost. Although we have no data
on the absolute numbers of northern Mexican gartersnakes in the United
States or Mexico, the best available science suggests that there are
far more individuals in Mexico than in the United States, based on the
more extensive range in Mexico and the current low density and number
of extant populations in the United States. Therefore, we have no
information to indicate that the loss of between 8 and 17 populations
of northern Mexican gartersnakes known in the United States is
biologically significant to the taxon as a whole.
In conclusion, we have determined that the gap in the range of the
northern gartersnake that would be caused by the loss of the United
States population would not be significant because: (1) Loss of the
United States population would not constitute a substantial and
biologically important reduction of the range of the subspecies; (2)
the loss of the individuals in the United States would not be
biologically significant to the subspecies; and (3) we have not
identified any other reason why loss of the United States population
would result in a significant gap in the range of the subspecies.
Marked Differences in Genetic Characteristics. Within the
distribution of every species there exists a peripheral population, an
isolate or subpopulation of a species at the edge of the taxon's range.
Long-term geographic isolation and loss of gene flow between
populations is the foundation of genetic changes in populations
resulting from natural selection or change. Evidence of changes in
these populations may include genetic, behavioral, and/or morphological
differences from populations in the rest of the species' range. We have
no information to indicate that genetic differences exist between
populations of the northern Mexican gartersnake at the northern portion
of its range in the United States from those in Mexico. Therefore,
based on the genetic information currently available, the northern
Mexican gartersnake in the United States should not be considered
biologically or ecologically significant based simply on
[[Page 56234]]
genetic characteristics. Biological and ecological significance under
the DPS policy is always considered in light of Congressional guidance
(see Senate Report 151, 96th Congress, 1st Session) that the authority
to list DPS's be used ``sparingly'' while encouraging the conservation
of genetic diversity.
Whether the Population Represents the Only Surviving Natural
Occurrence of the Taxon. As part of a determination of significance,
our DPS policy suggests that we consider whether there is evidence that
the population represents the only surviving natural occurrence of a
taxon that may be more abundant elsewhere as an introduced population
outside its historic range. The northern Mexican gartersnake in the
United States is not the only surviving natural occurrence of the
subspecies. Consequently, this factor is not applicable to our
determination regarding significance.
Conclusion
Following a review of the available information, we conclude that
the northern Mexican gartersnake in the United States is not
significant to the remainder of the subspecies. We made this
determination based on the best available information, which does not
demonstrate that (1) these populations persist in an ecological setting
that is unique for the subspecies; (2) the loss of these populations
would result in a significant gap in the range of the subspecies; and
(3) these populations differ markedly from populations of northern
Mexican gartersnake in Mexico in their genetic characteristics, or in
other considerations that might demonstrate significance. Further,
available information does not demonstrate that the life history and
behavioral characteristics of the northern Mexican gartersnake in the
United States is unique to the subspecies. Therefore, on the basis of
the best scientific and commercial information available, we find that
proposing to list a DPS for the northern Mexican gartersnake in the
United States is not warranted; these populations do not meet the
definition of a distinct population segment. We are not addressing the
third prong of the DPS policy (i.e. the population segment's
conservation status in relation to the Act's standards for listing)
since we find that the United States portion of the range of the
northern Mexican gartersnake does not qualify as a listable entity
pursuant to our DPS policy, as discussed above.
Significant Portion of the Range
In the petition to list the northern Mexican gartersnake, the
petitioners also requested that we consider listing the species
throughout its range based on its status in the United States. As
required by the Act, we have considered in this finding whether the
northern Mexican gartersnake is in danger of extinction ``in all or a
significant portion of its range'' as defined in the terms ``threatened
species'' and ``endangered species'' pursuant to section 3 of the Act.
In order to determine if Arizona constitutes a significant portion of
the range of the subspecies, we evaluate whether threats in this
geographic area imperil the viability of the subspecies as a whole due
to any biological importance of this portion of the subspecies range.
Based upon the best scientific information available, we find that the
extant populations in the United States are not considered a stronghold
for the subspecies, they do not represent core or important breeding
habitat, we are not aware of any unique genetic or behavioral
characteristics, and we are not aware that threats in this portion of
its range threaten the whole subspecies with extinction. Therefore, we
determine that the extant populations of the northern Mexican
gartersnake in Arizona do not constitute a significant portion of the
range of the subspecies because there is no particular characteristic
to any segment within this portion of its range that would render it
biologically more significant to the taxon as a whole than other
portions of its current range.
We note that the court in Defenders of Wildlife v. Norton, 258 F.3d
1136 (9th Cir. 2001), appeared to suggest that a species could be in
danger of extinction in a significant portion of its range if there is
a ``major geographical area'' in which the species is no longer viable
but once was. Although we do not necessarily agree with the court's
suggestion, we have determined that the historical range of the
subspecies within the United States does not constitute a ``major
geographical area'' in this context. The portion of the northern
Mexican gartersnake's historical range in United States (20 to 30 percent)
constitutes a small percentage of the total range of the subspecies.
The petitioners also requested that we consider listing the species
throughout its range based on its rangewide status. Below we respond to
the petitioners request through our analysis of the five listing
factors for the United States and Mexico.
Summary of Factors Affecting the Northern Mexican Gartersnake
Section 4 of the Act (16 U.S.C. 1533), and implementing regulations
at 50 CFR 424, set forth procedures for adding species to the Federal
Lists of Endangered and Threatened Wildlife and Plants. Under section
4(a) of the Act, we may list a species on the basis of any of five
factors, as follows: (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 making this finding, information
regarding the status of, and threats to, the northern Mexican
gartersnake in relation to the five factors provided in section 4(a)(1)
of the Act is discussed below and summarized in Table 1 below.
Table 1.--Summary of Northern Mexican Gartersnake Status and Threats by
Population in United States
[All locations in Arizona unless otherwise specified.]
------------------------------------------------------------------------
Regional historical/
Population locality Current status current threats
------------------------------------------------------------------------
Gila River.................... Extirpated....... Considered extirpated
by nonnatives,
improper grazing,
recreation,
development,
groundwater pumping,
diversions,
channelization,
dewatering, road
construction/use,
wildfire,
intentional harm,
dams, prey base
reductions.
Gila and San Francisco Extirpated....... Considered extirpated
Headwaters in New Mexico. by nonnatives,
improper grazing,
recreation, prey
base reductions.
Lower Colorado River from Extirpated....... Considered extirpated
Davis Dam to International by nonnatives, prey
Border. base reductions,
recreation,
development, road
construction/use,
borderland security/
undocumented
immigration,
intentional harm,
dams.
[[Page 56235]]
San Pedro River in United Extirpated....... Considered extirpated
States. by nonnatives, prey
base reductions,
improper grazing,
groundwater pumping,
road construction/
use, borderland
security/
undocumented
immigrants,
intentional harm.
Santa Cruz River downstream of Extirpated....... Considered extirpated
the Nogales area of the by nonnatives, prey
International Border. base reductions,
improper grazing,
development,
groundwater pumping,
diversions,
channelization, road
construction/use,
borderland security/
undocumented
immigrants,
intentional harm,
contaminants.
Salt River.................... Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing,
recreation,
development,
diversions,
wildfire,
channelization, road
construction/use,
intentional harm,
dams.
Rio San Bernardino from Extirpated....... Considered extirpated
International Border to by nonnatives, prey
headwaters at Astin Spring base reductions,
(San Bernardino National borderland security/
Wildlife Refuge). undocumented
immigration,
intentional harm,
competition with
Marcy's checkered
gartersnake.
Agua Fria River............... Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing,
development,
recreation, dams,
road construction/
use, wildfire,
intentional harm.
Verde River upstream of Extirpated....... Considered extirpated
Clarkdale. by nonnatives, prey
base reductions,
improper grazing,
recreation,
development,
groundwater pumping,
diversions,
channelization, road
construction/use,
intentional harm.
Verde River from the Extirpated....... Considered extirpated
confluence with the Salt by nonnatives, prey
upstream to Fossil Creek. base reductions,
improper grazing,
recreation,
groundwater pumping,
diversions,
channelization, road
construction/use,
wildfire,
development,intentio
nal harm, dams.
Potrero Canyon/Springs........ Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing.
Tanque Verde Creek in Tucson.. Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing,
recreation,
development,
groundwater pumping,
road construction/
use, intentional
harm.
Rillito Creek in Tucson....... Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing,
recreation,
development,
groundwater pumping,
road construction/
use, intentional
harm.
Agua Caliente Spring in Tucson Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing,
recreation,
development,
groundwater pumping,
road construction/
use, intentional
harm.
Babocamari Cienega............ Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing.
Barchas Ranch, Huachuca Extirpated....... Considered extirpated
Mountain bajada. by nonnatives, prey
base reductions,
improper grazing,
borderland security/
undocumented
immigration,
intentional harm.
Parker Canyon Lake and Extirpated....... Considered extirpated
tributaries in the Canelo by nonnatives, prey
Hills. base reductions,
improper grazing,
recreation, road
construction/use,
borderland security/
undocumented
immigration,
intentional harm,
dams.
Oak Creek at Midgley Bridge... Extirpated....... Considered extirpated
by nonnatives, prey
base reductions,
improper grazing,
recreation,
development,
intentional harm.
Santa Cruz River/Lower San Extant........... Nonnatives, prey base
Rafael Valley (headwaters reductions, improper
downstream to International grazing, borderland
Border). security/
undocumented
immigration,
intentional harm.
Verde River from the Extant........... Nonnatives, prey base
confluence with Fossil Creek reductions, improper
upstream to Clarkdale. grazing, recreation,
development,
groundwater pumping,
diversions,
channelization, road
construction/use,
intentional harm,
dams.
Oak Creek at Page Springs..... Extant........... Nonnatives, prey base
reductions.
Tonto Creek from mouth of Extant........... Nonnatives, prey base
Houston Creek downstream to reductions, improper
Roosevelt Lake. grazing, recreation,
development,
diversions,
channelization, road
construction/use,
wildfire,
intentional harm,
dams.
Cienega Creek from headwaters Extant........... Nonnatives, prey base
downstream to the ``Narrows'' reductions, improper
just downstream of Apache grazing.
Canyon.
Pantano Wash (Cienega Creek) Extant........... Nonnatives, prey base
from Pantano downstream to reductions, improper
Vail. grazing, wildfire.
Upper Scotia Canyon in the Extant........... Nonnatives, prey base
Huachuca Mountains. reductions,
wildfire.
Audubon Research Ranch and Extant........... Nonnatives, prey base
vicinity near Elgin. reductions, improper
grazing.
Downstream portion of the Unknown.......... Nonnatives, prey base
Black River drainage from the reductions, improper
Paddy Creek confluence. grazing, recreation,
intentional harm.
[[Page 56236]]
Downstream portion of the Unknown.......... Nonnatives, prey base
White River drainage from the reductions, improper
confluence of the East/North. grazing, recreation,
road construction/
use, intentional
harm.
Big Bonito Creek.............. Unknown.......... Nonnatives, prey base
reductions, improper
grazing.
Lake O' Woods (Lakeside)...... Unknown.......... Nonnatives, prey base
reductions,
recreation,
development, road
construction/use,
intentional harm.
Spring Creek above confluence Unknown.......... Nonnatives, prey base
with Oak Creek. reductions,
development.
Bog Hole Wildlife Area........ Unknown.......... Nonnatives, prey base
reductions.
Upper 13 Tank, Patagonia Unknown.......... Nonnatives, prey base
Mountains bajada. reductions, improper
grazing.
Babocamari River.............. Unknown.......... Nonnatives, prey base
reductions, improper
grazing.
Arivaca Cienega............... Unknown.......... Nonnatives, prey base
reductions, improper
grazing, borderland
security/
undocumented
immigration,
intentional harm.
------------------------------------------------------------------------
Note: ``Extirpated'' means that there have been no northern Mexican
gartersnakes reported for a decade or longer at a site within the
historical distribution of the species, despite survey efforts, and
there is no expectation of natural recovery at the site due to the
presence of known or strongly suspected causes of extirpation.
``Extant'' means areas where the species is expected to reliably occur
in appropriate habitat as supported by museum records and/or recent,
reliable observations. ``Unknown'' means areas where the species is
known to have occurred based on museum records (mostly historical) but
access is restricted, and/or survey data is unavailable or
insufficient, or where threats could preclude occupancy. The
information used to develop this table can be found in the sources
listed below.
Sources: Hyatt undated, p. 71; Nickerson and Mays 1970, pp. 495, 503;
Hulse 1973, p. 278; Vitt and Ohmart 1978, p. 44; Hendrickson and
Minckley 1984, p. 131, 138-162; Meffe 1985, pp. 179-185; Rosen 1987,
p. 5; Ohmart et al. 1988, pp. 143-147, 150; Rosen and Schwalbe 1988,
Appendix I; 1995, p. 452; 1996, pp. 1-3; 1997, p. 1; 2002b, pp. 223-
227; 2002c, pp. 31, 70; Bestgen and Propst 1989, pp. 409-410; Clarkson
and Rorabaugh 1989, pp. 531-538; Marsh and Minckley 1990, p. 265;
Medina 1990, pp. 351, 358-359; Sublette et al. 1990, pp. 112, 243,
246, 304, 313, 318; Abarca and Weedman 1993, pp. 2, 6-12; Girmendonk
and Young 1993, pp. 45-52; Sullivan and Richardson 1993, pp. 35-42;
Stefferud and Stefferud 1994, p. 364; Bahre 1995, pp. 240-252; Hale et
al. 1995, pp. 138-140; Holm and Lowe 1995, pp. 5, 27-35, 37-38, 45-46;
Rosen et al. 1995, p. 254; 1996b, pp. 8-9; 2001, Appendix I; Sredl et
al. 1995a, p. 7; 1995b, p. 9; 1995c, p. 7; 2000, p. 10; Degenhardt et
al. 1996, p. 319; Fernandez and Rosen 1996, pp. 6-19, 52-56; Stromberg
et al. 1996, pp. 113-114, 123-128; Yuhas 1996; Drost and Nowak 1997,
p. 11; Weedman and Young 1997, pp. 1, Appendices B, C; Inman et al.
1998, Appendix B; Rinne et al. 1998, pp. 75-80; Nowak and Spille 2001,
pp. 11, 32-33; Esque and Schwalbe 2002, pp. 161-193; Nowak and Santana-
Bendix 2002, p. 39; Stromberg and Chew 2002, pp. 198, 210-213; Tellman
2002, p. 43; USFWS 2002a, pp. 40802-40804; 2002b, Appendix H; 2006,
pp. 91-105; Voeltz 2002, pp. 40, 45-81; Krueper et al. 2003, pp. 607,
613-614; Bonar et al. 2004, pp. 1-108; Forest Guardians 2004, p. 1;
Unmack and Fagan 2004, p. 233; Fagan et al. 2005, pp. 34-41; Olden and
Poff 2005, pp. 75, 82-87; Painter 2005; Philips and Thomas 2005; Webb
and Leake 2005, pp. 302, 305-310, 318-320; ADWR 2006; American Rivers
2006; Brennan and Holycross 2006, p. 123; Holycross et al. 2006, pp.
15-61; McKinnon 2006a, 2006b, 2006c, 2006d, 2006e; Paradzick et al.
2006, pp. 88-93, 104-110; Segee and Neeley 2006, Executive Summary,
pp. 5-7; 10-12, 15-16, 21-23.
In the discussions of Factors A through E below, we describe the
known factors that have contributed to the current status of the
northern Mexican gartersnake. The majority of this assessment is
specific to those factors that have contributed to its status in the
United States. The following discussion of these factors that pertain
to the status and threats to the northern Mexican gartersnake in Mexico
are mainly regional, or statewide, in scope because in many cases we
were unable to find specific information documenting that populations
of the northern Mexican gartersnake in Mexico are directly affected by
these threats. In some instances, we do include discussion on more
refined geographic areas of Mexico when supported by the literature.
However, many of the threats that affect the northern Mexican
gartersnake in the United States are also present in Mexico. Thus, the
relationship between the threats to the habitat and species in Mexico
may be similar to what we have documented in the United States.
A. The Present or Threatened Destruction, Modification, or Curtailment
of Its Habitat or Range
In the following discussion, we elaborate on the physical threats
to northern Mexican gartersnake habitats (i.e., riparian and aquatic
communities) that have occurred and continue to occur within the
distribution of the species in the United States and Mexico. Various
threats that have affected and continue to affect riparian and aquatic
communities include dams, diversions, groundwater pumping, introduction
of nonnative species (vertebrates, plants, and crayfish), woodcutting,
mining, contaminants, urban and agricultural development, road
construction, livestock grazing, wildfires, and undocumented
immigration (Hendrickson and Minckley 1984, p. 161; Ohmart et al. 1988,
p. 150; Bahre 1995, pp. 240-252; Medina 1990, p. 351; Sullivan and
Richardson 1993, pp. 35-42; Fleischner 1994, pp. 630-631; Hadley and
Sheridan 1995; Hale et al. 1995, pp. 138-140; DeBano and Neary 1996,
pp. 73-75; Rinne and Neary 1996, p. 135; Stromberg et al. 1996, pp.
124-127; Girmendock and Young 1997, pp. 45-52; Rinne et al. 1998, pp.
7-11; Belsky et al. 1999, pp. 8-12; Esque and Schwalbe 2002, pp. 165,
190; Hancock 2002, p. 765; Voeltz 2002, pp. 87-88; Webb and Leake 2005,
pp. 305-308; Holycross et al. 2006, pp. 52-61; McKinnon 2006a, 2006b,
2006c, 2006d, 2006e; Paradzick et al. 2006, pp. 88-93; Segee and Neeley
1996, Executive Summary, pp. 10-12, 21-23). These activities and their
effects on the northern Mexican gartersnake are discussed in further
detail below.
It is important to recognize that in most areas where northern
Mexican gartersnakes historically or currently occur, two or more
threats may be acting synergistically in their influence on the
suitability of those habitats or on the northern Mexican gartersnake
itself. In our assessment of the status of these habitats, discussion
of the role that nonnative species introductions have had on habitat
suitability is critical. However, we provide that discussion under
``Factor C. Disease and Predation'' due to the intricate and complex
relationship nonnative species have with respect to direct and indirect
pressures applied to the northern
[[Page 56237]]
Mexican gartersnake and to its native prey base.
Threats to Riparian and Aquatic Biological Communities in the
United States. The modification and destruction of aquatic and riparian
communities in the post-settlement arid southwestern United States is
well documented and apparent in the field (Medina 1990, p. 351;
Sullivan and Richardson 1993, pp. 35-42; Fleischner 1994, pp. 630-631;
Stromberg et al. 1996, pp. 113, 123-128; Girmendock and Young 1997, pp.
45-52; Belsky et al. 1999, pp. 8-12; Webb and Leake 2005, pp. 305-310;
Holycross et al. 2006, pp. 52-61). Several threats have been identified
in the decline of many native riparian flora and fauna species through
habitat modification and destruction as well as nonnative species
introductions. Researchers agree that the period from 1850 to 1940
marked the greatest loss and degradation of riparian and aquatic
communities in Arizona, which were caused by anthropogenic (human) land
uses and the primary and secondary effects of those uses (Stromberg et
al. 1996, p. 114; Webb and Leake 2005, pp. 305-310). Many of these land
activities continue today and are discussed at length below. An
estimated one-third of Arizona's pre-settlement wetlands have dried or
have been rendered ecologically dysfunctional (Yuhas 1996).
Modification and Loss of Cienegas in the United States. Cienegas
are particularly important habitat for the northern Mexican gartersnake
and are considered ideal for the species (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 soils.'' Many of these
unique communities of the southwestern United States, and Arizona in
particular, have been lost in the past century to streambed
modification, improper livestock grazing, cultural impacts, stream flow
stabilization by upstream dams, channelization, and stream flow
reduction from groundwater pumping and 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 along
many southwestern streams, including the San Pedro River. Conservation
of the remaining natural cienegas in Arizona will be contingent on
their protection from severe flooding and from lowering of groundwater
levels (Hendrickson and Minckley 1984, p. 169).
Many sub-basins where cienegas have been severely modified or lost
entirely overlap, wholly or partially, 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 possessed several natural
cienegas with luxuriant 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 heavy 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).
Urban and Rural Development in the United States. 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 watershed (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). 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, Gila, and Salt rivers,
respectively). Urbanization and development of these areas, along with
the introduction of nonnative species, are largely responsible for the
extirpation of the northern Mexican gartersnake from these areas.
Urbanization on smaller scales can also impact habitat suitability
and the prey base for the northern Mexican gartersnake. Medina (1990,
pp. 358-359) concluded that perennial streams had greater tree
densities in all diameter size classes of Arizona alder and box elder
(Acer negundo) as compared to ephemeral reaches where small diameter
trees were absent. Small diameter trees assist the northern Mexican
gartersnake by providing additional habitat complexity and cover needed
to reduce predation risk and enhance the usefulness of areas for
thermoregulation. Regional development and subsequent land use changes,
spurred by increasing populations, along lower Tonto Creek and within
the Verde Valley where northern Mexican gartersnakes are extant
continue to threaten this snake's habitat and affect the habitat's
suitability for the northern Mexican gartersnake and its prey species
(Girmendock and Young 1997, pp. 45-52; Voeltz 2002, pp. 58-59, 69-71;
Paradzick et al. 2006, pp. 89-90). Holycross et al. (2006, pp. 53, 56)
recently documented adverse effects to northern Mexican gartersnake
habitat in the vicinity of Rock Springs along the Agua Fria River and
also throughout the Verde Valley along the Verde River.
The effects of urban and rural development are expected to increase
as populations increase. Consumer interest in second home and/or
retirement real estate investments has increased significantly in
recent times within the southwestern United States. Medina (1990, p.
351) points out that many real estate investors are looking for
aesthetically scenic, mild climes to enjoy seasonally or year-round and
hence choose to develop pre- or post-retirement properties that are
within or adjacent to riparian areas due to their aesthetic appeal and
available water. Arizona increased its population by 394 percent from
1960 to 2000, and is second only to Nevada as the fastest growing State
in terms of human population (SSDAR 2000). Over the same time period,
population growth rates in Arizona counties where the northern Mexican
gartersnake historically occurred or may still be extant have varied by
county but are no less remarkable: 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 (2004 percent) (SSDAR 2000). Population growth
trends in Arizona,
[[Page 56238]]
and Maricopa County in particular, are expected to continue into the
future. The Phoenix metropolitan area, founded in part due to its
location at the junction of the Salt and Gila rivers, is a population
center of 3.63 million people. The Phoenix metropolitan area is the
sixth largest in the United States and resides in the fastest growing
county in the United States since the 2000 census (Arizona Republic 2006).
Development growth predictions have also been made for
traditionally rural portions of Arizona. The populations of developing
cities and towns of the Verde watershed are expected to more than
double in the next 50 years, which may pose exceptional threats to
riparian and aquatic communities of the Verde Valley where northern
Mexican gartersnakes occur (Girmendock and Young 1993, p. 47; American
Rivers 2006; Paradzick et al. 2006, p. 89). Communities in Yavapai and
Gila counties such as the Prescott-Chino Valley, Strawberry, Pine, and
Payson have all seen rapid population growth in recent years. For
example, the population in the town of Chino Valley, at the headwaters
of the Verde River, has grown by 22 percent between 2000 and 2004; Gila
County, which includes reaches of the Salt, White, and Black rivers and
Tonto Creek, grew by 20 percent between 2000 and 2003 (http://
www.census.gov). The upper San Pedro River is also the location of
rapid population growth in the Sierra Vista-Huachuca City-Tombstone
area (http://www.census.gov). All of these communities are near or
within the vicinity of historical or extant northern Mexican
gartersnake populations.
Road Construction, Use, and Maintenance in the United States. Roads
cover approximately one percent of the land area in the United States,
but negatively affect 20 percent of the habitat and biota in the United
States (Angermeier et al. 2004, p. 19). Roads pose unique threats to
herpetofauna (reptiles and amphibians) and specifically to species like
the northern Mexican gartersnake, its prey base, and the habitat where
it occurs through: (1) Fragmentation, modification, and destruction of
habitat; (2) an 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 and/or inhibition of reproduction; (7)
contributions of pollutants to riparian and aquatic communities; and
(8) population sinks through direct mortality (Rosen and Lowe 1994, pp.
146-148; Waters 1995, p. 42; 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).
Construction and maintenance of roads and highways near riparian
areas can be a source of sediment and pollutants (Waters 1995, p. 42;
Wheeler et al. 2005, pp. 145, 148-149). Sediment can adversely affect
fish populations used as prey by the northern Mexican gartersnake by
(1) interfering with respiration; (2) reducing the effectiveness of
visually-based hunting behaviors; and (3) filling in interstitial
spaces of the substrate which reduces reproduction and foraging success
of fish interfering with respiration, and restricting reproduction and
foraging of fish. Excessive sediment also fills in intermittent pools
required for amphibian prey reproduction and foraging. Fine sediment
pollution in streams impacted by highway construction without the use
of sediment control structures was 5 to 12 times greater than control
streams. Sediment can lead to several effects in resident fish species
used by northern Mexican gartersnakes as prey species, which can
ultimately cause the northern Mexican gartersnake's increased direct
mortality, reduced reproductive success, lower overall abundance, lower
species diversity, and reductions in food base as documented by Wheeler
et al. (2005, p. 145). The underwater foraging ability of northern
Mexican gartersnakes can also be directly compromised by excessive
turbidity caused by sedimentation of water bodies. Metal contaminants,
including iron, zinc, lead, cadmium, nickel, copper, and chromium, are
bioaccumulative) and are associated with highway construction and use
(Foreman and Alexander 1998, p. 220; Hopkins et al. 1999, p. 1260;
Campbell et al. 2005, p. 241; Wheeler et al. 2005, pp. 146-149). 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 and lead to adverse health affects.
Several studies have addressed the effects of bioaccumulative
substances on watersnakes. We find these studies relevant because
watersnakes and gartersnakes have very similar life histories and prey
bases and therefore, the effects from contamination of their habitat
from bioaccumulative agents are expected to have similar effects.
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 food item, the central stoneroller (fish)
(Campostoma anomalum). Metals, in trace amounts, affect the structure
and function of the liver and kidneys of vertebrates and may also act
as neurotoxins, affecting nervous system function (Rainwater et al.
2005, p. 670). Metals may also be sequestered in the skin of reptiles,
but this effect is tempered somewhat by ecdysis (the regular shedding
or molting of the skin) (Burger 1999, p. 212). Hopkins et al. (1999, p.
1261) found that metals may even interfere with metabolic rates of
banded watersnakes (Nerodia fasciata), altering the allocation of
energy between maintenance and reproduction, reducing the efficiency of
energy stores, and forcing individuals to forage more often, which
increases activity costs (the energy expended in hunting which effects
the net nutritional intake of an organism) and predation risk.
Snakes of all species are particularly vulnerable to mortality when
they attempt to cross roads. There are several reasons for this
phenomenon. First, all snakes are thigmotherms (animals that derive
heat from warm surfaces), which often compels them to slow down or even
stop and rest on road surfaces that have been warmed by the sun as they
attempt to cross (Rosen and Lowe 1994, p. 143). Additionally, many
species of snakes are active when traffic densities are greatest, as is
the case with gartersnakes, which are generally diurnal (active during
daylight hours) (Rosen and Lowe 1994, p. 147). 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, which highlights the seasonal variability in surface activity
of this snake, and many other species of reptiles. Perhaps the most
common factor in road mortality of snakes is the propensity for drivers
to intentionally run over snakes, which generally make easy targets
because they usually cross roads at a perpendicular angle (Klauber
1956, p. 1026; Langley et al. 1989, p. 47; Shine et al. 2004, p. 11).
This driving behavior is exacerbated by the general animosity that
humans have toward snakes in general in modern-day society (Ernst and
Zug 1996, p. 75; Green 1997 pp. 285-286). In fact, Langley et al.
(1989, p. 47) conducted an experiment on the propensity for drivers to
hit reptiles on the road using turtle and snake models and found that many
[[Page 56239]]
people have a greater desire to hit a snake on the road than any other
animal; several drivers actually stopped and backed-over the snake
mimic to ensure it was dead. Roe et al. (2006, p. 161) conclude that
mortality rates due to roads are higher in vagile (mobile) species,
such as gartersnakes (active hunters), than those of more sedentary
species, such as the North American pit vipers in the genera
Agkistrodon, Sistrurus, and Crotalus, which more commonly employ sit-
and-wait foraging strategies. Roads that bisect wetland communities
also act as mortality sinks in the dispersal or migratory movements of
snakes (Roe et al. 2006, p. 161). The effect of road mortality of
snakes becomes most significant in the case of small, highly fragmented
populations where the chance removal of mature females from the
population may appreciably degrade the viability of a population.
Roads create easy access to areas previously infrequently visited
or inaccessible to humans, increasing the frequency and significance of
anthropogenic threats to riparian areas and fragmenting the landscape,
which may genetically isolate herpetofaunal populations (Rosen and Lowe
1994, pp. 146-148; Andrews and Gibbons 2005, p. 772).
While snakes of all species may suffer direct mortality from
attempting to cross roads, Andrews and Gibbons (2005, pp. 777-779)
found that many individuals of small, diurnal snake species avoid open
areas (e.g., roads) instinctively in order to lower predation rates,
which represents a different type of threat from roads. Shine et al.
(2004, p. 9) found that the common gartersnake typically changed
direction when encountering a road. These avoidance behaviors by
individuals aversive to crossing roads affect movement patterns and may
ultimately affect reproductive output within populations (Shine et al.
2004, pp. 9, 17-19). This avoidance behavior has been observed in the
common gartersnake (Thamnophis sirtalis), a sister taxon to the Mexican
gartersnake with similar life histories and behavior (Shine et al.
2004, p. 9). In our discussion and as evidenced by the literature we
reviewed on the effect of roads on snake movements, we acknowledge the
individuality of snakes in their behaviors towards road crossings in
that roads may affect a snake's movement behavior by a variety of means
and that generalizing these resultant behaviors does not adequately
address this variability.
In addition to altering the movement patterns of some snakes, roads
can interfere with the male gartersnake's olfactory-driven ability to
follow the pheromone trails left by receptive females (Shine et al.
2004, pp. 17-18). This effect to the male's ability to trail females
may exacerbate the effects of low population density and fragmentation
that affect several species of snakes, including the northern Mexican
gartersnake. Furthermore, roads can facilitate an increase in the
distance traveled by male snakes seeking receptive females, which
increases exposure to predation and subsequently increases mortality
rates (Shine et al. 2004, pp. 18-19). Although the northern Mexican
gartersnake was not the subject of the 2004 Shine et al. study, similar
responses can be expected in the northern Mexican gartersnake because
its life history is similar to the, study's subject species (i.e., the
common gartersnake).
Roads tend to adversely affect aquatic breeding anuran (frog and/or
toad) populations more so than other species due to their activity
patterns, population structures, and preferred habitats (Hels and
Buchwald 2001, p. 331). Carr and Fahrig (2001, pp. 1074-1076) found
that populations of highly mobile anuran species such as leopard frogs
(Rana pipiens) were affected more significantly than more sedentary
species and that population persistence can be at risk depending on
traffic densities, which may adversely affect the prey base for
northern Mexican gartersnakes because leopard frogs are a primary prey
species.
Recreation in the United States. As discussed above, population
growth trends are expected to continue into the future. Expanding
population growth leads to higher recreational use of riparian areas.
Riparian areas located near urban areas are vulnerable to the effects
of increased recreation with predictable changes in the type and
intensity of land use following residential development. An example of
such an area within the existing distribution of the northern Mexican
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 neonates.
Increased human visitation of occupied habitat also increases the
potential for human-gartersnake interactions, which frequently does not
bode well for snakes, as it often leads to their capture, injury, or
death of the snake due to the lay person's fear of 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).
Groundwater Pumping, Surface Water Diversions, and Drought in the
United States. Increased urbanization and population growth results in
an increase in the demand for water and, therefore, water development
projects. Collier et al. (1996, p. 16) mention that water development
projects are one of two main causes of decline of native fish in the
Salt and Gila rivers of Arizona. Municipal water use in central Arizona
has increased by 39 percent in the last 8 years (American Rivers 2006).
Water for development and urbanization is often supplied by 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 desiccation 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). If complete disconnection occurs, the
hyporheic zone could be adversely affected. The hyporheic zone can
promote ``hot spots'' of productivity where groundwater upwelling
occurs by producing 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). Changes to the duration and timing of
upwelling can potentially lead to localized extinctions in biota
(Boulton and Hancock 2006, p. 139).
To varying degrees, the effects of groundwater pumping on surface
water flow and riparian communities have been observed in the Santa
Cruz, San Pedro, and Verde rivers as a result of groundwater demands of
Tucson, Sierra
[[Page 56240]]
Vista, and the rapidly growing Prescott Valley, respectively (Stromberg
et al. 1996, pp. 113, 124-128; Rinne et al. 1998, p. 9; Voeltz 2002,
pp. 45-47, 69-71). 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 being
currently dominated by woody species more tolerant of declining water
tables due to their associated deeper rooting depths.
The full effects of largescale groundwater pumping associated with
the proposed Big Chino Water Ranch Project and its associated 30-mile
(48 km), 36-in (91-cm) diameter pipeline have yet to be realized in the
Verde River (McKinnon 2006c). This groundwater pumping and inter-basin
transfer project is projected to deliver 2.8 billion gallons of
groundwater annually from the Big Chino sub-basin aquifer to the
rapidly growing area of Prescott Valley for municipal use (McKinnon
2006c). The Big Chino sub-basin provides 86 percent of the baseflow to
the upper Verde River (American Rivers 2006; McKinnon 2006a). The
potential for this project to obtain funding and approval for
implementation has placed the Verde River on American River's ``Ten
Most Endangered Rivers List (of 2006)'' (American Rivers 2006). This
potential reduction or loss of baseflow in the Verde River could
seasonally dry up large reaches and/or adversely affect the riparian
community and the suitability of the habitat for extant populations of
the northern Mexican gartersnake and its prey species in that area.
Within the Verde River watershed, and particularly within the Verde
Valley where the northern Mexican gartersnake remains extant, several
other activities continue to threaten surface flows (Rinne et al. 1998,
p. 9; 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, which may have supported the
northern Mexican gartersnake (Girmendock and Young 1993, pp. 45-47;
Sullivan and Richardson 1993, pp. 38-39; Paradzick et al. 2006, pp.
104-110). Groundwater pumping in Tonto Creek regularly eliminates
surface flows during parts of the year (Abarca and Weedman 1993, p. 2).
The upper Gila River is also threatened by diversions and water
allocations. In New Mexico, a proposed water project that resulted from
a landmark Gila River water settlement in 2004 allows New Mexico the
right to withhold 4.5 billion gallons of surface water every year
(McKinnon 2006d). If this proposed water diversion project is
implemented, in dry years, currently perennial reaches of the upper
Gila River will dry completely which removes all suitability of this
habitat for the northern Mexican gartersnakes and a host of other
riparian and aquatic species (McKinnon 2006d).
Further evidence of the threat of groundwater depletion can be
found in the management activities of the Arizona Department of Water
Resources (ADWR). ADWR manages water supplies in Arizona and has
established five Active Management Areas (AMA) across the state (ADWR
2006). An AMA is established by ADWR when an area's water demand has
exceeded the groundwater supply and an overdraft has occurred.
Geographically, all five AMAs overlap the historical distribution of
the northern Mexican gartersnake in Arizona and provide further
evidence of the role groundwater pumping has had and continues to have
on historical and occupied northern Mexican gartersnake habitat. Such
overdrafts are capable of adversely impacting surface water flow of
streams that are hydrologically connected to the aquifer under stress
and are often exacerbated by the ever-growing number of surface water
diversions for various purposes.
In order to accommodate the needs of rapidly growing rural and
urban populations, surface water is commonly diverted to serve many
industrial and municipal uses. These diversions have dewatered large
reaches of once perennial or intermittent streams, adversely affecting
northern Mexican gartersnake habitat throughout its range in Arizona
and New Mexico. Many tributaries of the Verde River are permanently or
seasonally dewatered by diversions for agriculture (Paradzick et al.
2006, pp. 104-110).
The effects of the water withdrawals discussed above may be
exacerbated by the current, long-term drought facing the arid
southwestern United States. Philips and Thomas (2005) provided
streamflow records that indicate that the drought Arizona experienced
between 1999 and 2004 was the worst drought since the early 1940s and
possibly earlier. Ongoing drought conditions have depleted recharge of
aquifers and decreased baseflows in the region. While drought periods
have been relatively numerous in the arid Southwest according to
recorded history from the mid-1800s to the present, the effects of
anthropogenic threats on riparian and aquatic communities have
compromised the ability of these communities to function under the
additional stress of prolonged drought conditions. Holycross et al.
(2006, pp. 52-53) recently documented the effects of drought on
northern Mexican gartersnake habitat in the vicinity of Arcosante along
the Agua Fria River and at Big Bug Creek where the streams were completely
dry and therefore unsuitable northern Mexican gartersnake habitats.
Improper Livestock Grazing in the United States. Poorly managed
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; Waters
1995, pp. 22-24; Pearce et al. 1998, p. 307; Belsky et al. 1999, p. 1).
Livestock grazing, as a resource use on public and private lands, has
more than doubled quantitatively in 50 years; the number of cattle
being grazed in the western United States increased from 25.5 million
head in 1940, to 54.4 million head in 1990 (Belsky et al. 1999, p. 3).
Effects of improper livestock management on riparian and aquatic
communities have spanned from early settlement to modern day. Some
historical accounts of riparian area conditions in Arizona elucidate
early effects of poor livestock management. Cheney et al. (1990, pp. 5,
10) provide historical accounts of the early adverse effects of
improper livestock management in the riparian zones and adjacent
uplands of the Tonto National Forest and in south-central Arizona.
These accounts describe the removal of riparian trees for preparation
of livestock use and substantial changes to flow regimes accentuated by
observed increases in runoff and erosion rates. Such accounts of
riparian conditions within the historical distribution of the northern
Mexican gartersnake in Arizona contribute to the understanding of when
declines in abundance and distribution may have occurred and the causes
for subsequent fragmentation of populations and widespread
extirpations.
In the recent past, riparian and aquatic communities have been
negatively impacted by poor livestock management (e.g., overgrazing,
uncontrolled access to riparian areas,
[[Page 56241]]
improper pasture rotation, no monitoring of use, etc.) within several
watersheds that the northern Mexican gartersnake historically occupied,
and in some cases, poor livestock management may constitute the
greatest impact to riparian vegetation. The specific ways in which
improper livestock grazing can adversely affect northern Mexican
gartersnakes and contribute to their decline is discussed below.
Watersheds where improper grazing has been documented as a contributing
factor of northern Mexican 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; Girmendock and Young 1997, p. 47; Voeltz 2002, pp. 45-81; Krueper
et al. 2003, pp. 607, 613-614; Holycross et al. 2006, pp. 52-61;
McKinnon 2006d, 2006e; Paradzick et al. 2006, pp. 90-92). Holycross et
al. (2006, pp. 53-55, 58) recently documented adverse effects from
improper livestock grazing on northern Mexican gartersnake habitat
along the Agua Fria from EZ Ranch to Bloody Basin Road, along Dry Creek
from Dugas Road to Little Ash Creek, along Little Ash Creek from Brown
Spring to Dry Creek, along Sycamore Creek in the vicinity of its
confluence with the Verde River, and on potential northern Mexican
gartersnake habitat along Pinto Creek at the confluence with the West
Fork of Pinto Creek. In southeastern Arizona, there have been
observations of effects to the vegetative community suggesting that
livestock grazing activities continue to adversely affect extant
populations of northern Mexican gartersnakes by reducing or eliminating
cover required by the northern Mexican gartersnake for
thermoregulation, protection from predation, and foraging (Hale 2001,
pp. 32-34, 50, 56).
Poor livestock management causes a decline in diversity, abundance,
and species composition of riparian herpetofauna communities from
direct or indirect threats to the prey base, the habitat, or to the
northern Mexican gartersnake itself from: (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; and (5) a rise in water
temperatures to levels lethal to larval stages of amphibian and fish
development (Szaro et al. 1985, p. 362; Schulz and Leininger 1990, p.
295; Belsky et al. 1999, pp. 8-11). Improper livestock grazing may also
lead to desertification (the process of becoming arid land or desert as
a result of land mismanagement or climate change) due to a loss in soil
fertility from erosion and gaseous emissions spurred by a reduction in
vegetative ground cover (Schlesinger et al. 1990, p. 1043). Stock tanks
may facilitate the spread of nonnative species when nonnative species
of fish, amphibians, and crayfish are intentionally or unintentionally
stocked by anglers and private landowners (Rosen et al. 2001, p. 24).
Specific attributes of ecosystems, such as composition, function, and
structure, have been documented as being altered by improper livestock
management through a variety of means including: (1) Decreasing the
density and biomass of individual species, reducing species richness,
and changing biological community organization; (2) interfering with
nutrient cycling and ecological succession; and (3) changing vegetation
stratification, contributing to soil erosion, and decreasing
availability of water to biotic communities (Fleischner 1994, p. 631).
The management of stock tanks is an important consideration for
northern Mexican gartersnakes. Stock tanks can be intermediary
``stepping stones'' in the dispersal of nonnative species from larger
source populations to new areas (Rosen et al. 2001, p. 24).
Additionally, dense bank and aquatic vegetation is an important habitat
characteristic for the northern Mexican gartersnake that can be
affected if the impoundment is poorly managed, which may lead to
trampling or overgrazing of the bankside vegetation. Poor management
may also favor nonnative predators of the northern Mexican gartersnake
(Rosen and Schwalbe 1988, pp. 47, 32). Alternatively, well-managed
stock tanks can provide habitat suitable for northern Mexican
gartersnakes both structurally and in terms of prey base, especially
when the tank remains devoid of nonnative species while supporting
native prey species; provides adequate vegetation cover; and provides
reliable water sources in periods of prolonged drought. Given these
benefits of well-managed stock tanks, we believe well-managed stock
tanks may be an important component to northern Mexican gartersnake
conservation.
A key to proper livestock management appears to be increasing the
distribution of cattle across the entire grazing space. 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 poorly managed cattle
to remain within or adjacent to riparian communities. Trimble and
Mendel (1995, p. 243) stated that ``Cows, unlike sheep, appear to love
water and spend an inordinate amount of time together lounging in
streams and ponds, especially in summer (surface-active season for
reptiles and amphibians), sometimes going in and coming out several
times in the course of a day.'' Expectedly, this behavior is more
pronounced in more arid regions (Trimble and Mendel 1995, p. 243). In
one rangeland study, it was concluded that 81 percent of the vegetation
that was removed by cattle was from a riparian area which amounted to
only two percent of the total grazing space (Trimble and Mendel 1995,
p. 243). Another study reported that grazing rates were 5 to 30 times
higher in riparian areas than on the uplands which may be due in part
to several factors: (1) Higher forage volume and palatability of
species in riparian areas; (2) water availability; (3) the close
proximity of riparian areas to the best upland grazing sites; and (4)
microclimatic features such as cooler temperatures and shade (Trimble
and Mendel 1995, p. 244).
The northern Mexican gartersnake uses riparian herbaceous
vegetation for cover, thermoregulation, and foraging. Clary and Webster
(1989, p. 1) noted that excessive grazing and trampling from poor
livestock management can affect riparian and stream communities by
reducing or eliminating this vegetation, causing channel aggradation or
degradation, causing widening or incisement of stream channels, and
changing streambank morphology, with the cumulative result of lowering
corresponding water tables. In support of findings made by Fleischner
(1994, pp. 631-632), these effects can largely be attributed to the
tendency of livestock in the arid Southwest to spend a
disproportionately longer time in riparian areas than in upland range
pasture (5-30 times longer, comparatively), which leads to overgrazing
of the riparian vegetation (Clary and Medin 1990, p. 1). However, even
when livestock's access to riparian areas is restricted, poor livestock
management in the uplands leads to soil compaction and decreased
filtering capacity of vegetation. These effects increase the speed and
amount of runoff from the uplands, which contributes heightened,
unnatural amounts of sediment in aquatic habitat. This damages the
suitability of that habitat and fills in pools, which affects their
permanency and suitability for many prey species of the northern Mexican
[[Page 56242]]
gartersnake (Sartz and Tolsted 1974, p. 354; Weltz and Wood 1986, pp.
367-368; Orodho et al. 1990, p. 9; Trimble and Mendel 1995, pp. 235-
236; Pearce et al. 1998, p. 302). The response of riparian herbaceous
vegetation after the removal of cattle was documented as dramatic, with
a four to six fold increase in density, as observed in the upper San
Pedro River (Krueper et al. 2003, pp. 607, 613-614). Schulz and
Leininger (1990, p. 295) also remarked that riparian ecosystems can
improve quickly when livestock are removed.
As stated previously, dense vegetative cover is an essential
component to habitat suitable for the northern Mexican gartersnake for
several reasons (Szaro et al. 1985, p. 364; Rosen and Schwalbe 1988, p.
47). The removal or severe alteration of this habitat component
significantly affects the foraging success and heightens the predation
risk of the northern Mexican gartersnake. Small, isolated populations
of northern Mexican gartersnakes that use stock tanks as refugia may be
extirpated within 1 year of vegetation removal (Rosen and Schwalbe
1988, p. 33). Northern Mexican gartersnake populations that occur in
isolated wetlands or stock tanks are not likely to recolonize naturally
(i.e. without reestablishment efforts) once extirpated due to the
species' tendency to avoid long overland movements (Rosen and Schwalbe
1988. p. 33).
Szaro et al. (1985, p. 360) assessed the effects of improper
livestock management on the same stream on a sister taxon. They 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 complemented by higher
amounts of cover from organic debris from ungrazed shrubs that
accumulates 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). The resultant
extirpation risk of amphibian populations as a prey base for northern
Mexican gartersnakes by direct mortality is governed by the relative
isolation of the amphibian population, the viability of that
population, and the propensity for stochastic events such as wildfires.
Livestock grazing within habitat occupied by northern Mexican
gartersnakes can result in direct mortality of individual gartersnakes
as observed in a closely related taxon on the Apache-Sitgreaves
National Forest. In that instance, a black-necked gartersnake
(Thamnophis cyrtopsis cyrtopsis) had apparently been killed by
trampling hoof action of cattle along the shore of a stock tank within
an actively grazed allotment (Chapman 2005). This event was not
observed first-hand, but was supported by postmortem photo
documentation of the physical injuries to the specimen and the location
of the carcass among a dense cluster of hoof tracks along the shoreline
of the stock tank. It is also unlikely that a predator would kill the
snake and leave it uneaten. While this type of direct mortality of
gartersnakes has long been suspected by agency biologists and academia,
this may be the first recorded observation of direct mortality of a
gartersnake due to livestock trampling. We expect this type of direct
mortality to be uncommon but significant in the instance of a
fragmented population with a skewed age-class distribution and low to
no recruitment as currently observed in many northern Mexican
gartersnake populations in the United States. In these circumstances,
the loss of one or more adults, most notably reproductive females, may
lead directly to extirpation of the species from a given site with no
expectation of recolonization.
Our analysis of the best available scientific and commercial
information available indicates that adverse effects from improper
livestock management on the northern Mexican gartersnake, its habitat,
and its prey base can be significant. However, we recognize that well-
managed grazing can occur with limited effects to this species when
management emphasis is directed to moderated access restrictions for
occupied habitat combined with the use of remote drinkers
(containerized water sources supplied by water pumped from a nearby
source) as well as other livestock management protocols that lessen the
effect of vegetation disturbance and removal adjacent to occupied
habitat by increasing the distribution of cattle across an allotment.
Lastly, as previously stated, we also recognize the value of well-
managed stock tanks in the conservation of northern Mexican gartersnakes.
Catastrophic Wildfires in the United States. 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 the current effects of fire management
policies on aquatic communities in Madrean-type ecosystems 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 devastating
wildfires. The effects of these catastrophic wildfires include the
removal of vegetation, the degradation of watershed condition, altered
stream hydrographs, and increased sedimentation of streams. These
effects can harm fish communities, as observed in the 1990 Dude Fire,
in which corresponding ash flows decimated some fish populations in
Dude Creek and the East Verde River (Voeltz 2002, p. 77). These effects
can significantly lessen the prey base for northern Mexican
gartersnakes and could lead to direct mortality in the case of fires
that are within occupied habitat.
Fire has also become an increasingly significant threat in lower
elevation communities as well. Esque and Schwalbe (2002, pp. 180-190)
discuss the effect of wildfires in the upper and lower subdivisions of
Sonoran desertscrub where the northern Mexican gartersnake historically
occurred. The widespread invasion of nonnative annual grasses, such as
brome species (Bromus sp.) and Mediterranean grasses (Schismus sp.),
appear to be largely responsible for altered fire regimes that have
been observed in these communities, which are not adapted to fire
(Esque and Schwalbe 2002, p. 165). In areas comprised entirely of
native species, ground vegetation density is mediated by barren spaces
that do not allow fire to carry itself across the landscape. However,
in areas where nonnative grasses have become established, the fine fuel
load is continuous, and fire is capable of spreading quickly and
efficiently (Esque and Schwalbe 2002, p. 175). After disturbances such
as fire, brome grasses may exhibit dramatic population
[[Page 56243]]
explosions, which hasten their effect on native vegetative communities.
Additionally, with increased fire frequency, these population
explosions ultimately lead to a type-conversion of the vegetative
community from desertscrub to grassland (Esque and Schwalbe 2002, pp.
175-176). Fires carried by the fine fuel loads created by nonnative
grasses often burn at unnaturally high temperatures, which may result
in soils becoming hydrophobic (water repelling), exacerbate sheet
erosion, and contribute large amounts of sediment to receiving water
bodies, thereby affecting the health of the riparian community (Esque
and Schwalbe 2002, pp. 177-178). The siltation of isolated, remnant
pools in intermittent streams has significant effects on lower-
elevation species, as observed in lowland leopard frogs and native
fish, important prey species for northern Mexican gartersnakes (Esque
and Schwalbe 2002, p. 190).
Undocumented Immigration and International Border Enforcement and
Management in the United States. Undocumented immigrants attempt to
cross the International border from Mexico into the United States in
areas historically or currently occupied by the northern Mexican
gartersnake. This method of immigration and the corresponding efforts
to enforce U.S. border laws and policies have been occurring for many
decades with increasing intensity and have resulted in unintended
adverse effects to biotic communities in the border region. During the
warmest months of the year, many attempted border crossings occur in
riparian areas that serve to provide shade, water, and cover. Increased
U.S. border enforcement efforts that began in the early 1990s in
California and Texas have resulted in concentrated levels of attempted
undocumented immigrant crossings into Arizona (Segee and Neeley 2006,
p. 6).
Riparian habitats that historically supported or may currently
support northern Mexican gartersnakes in the San Bernardino National
Wildlife Refuge, the San Pedro River corridor, the Santa Cruz River
corridor, the lower Colorado River corridor, and along many smaller
streamside and canyon bottom areas within Cochise, Santa Cruz, and Pima
counties have high levels of undocumented immigrant traffic (Segee and
Neeley 2006, Executive Summary, pp. 10-12, 21-23).
Use of new roads and trails from immigration and enforcement
activities, as well as the construction, use, and maintenance of
enforcement infrastructure (i.e., fences, walls, and lighting systems),
leads to compaction of streamside soils, and the destruction and
removal of riparian vegetation necessary as cover for the northern
Mexican gartersnake. These activities also serve as a source of
additional sediment to streams that affect their suitability as habitat
for prey species of the northern Mexican gartersnake and affect the
suitability and availability of pool habitats by filling them in with
sediment. Riparian areas along the upper San Pedro River have been
impacted by out of control fires that undocumented immigrants likely
started to keep warm and/or prepare food (Segee and Neeley 2006, p.
23). There also remains the threat of pursuit, capture, and death of
northern Mexican gartersnakes when they are encountered by undocumented
immigrants and border enforcement personnel in high use areas due to
the snake's stigma in society (Rosen and Schwalbe 1988, p. 43; Ernst
and Zug 1996, p. 75; Green 1997, pp. 285-286; Nowak and Santana Bendix
2002, p. 39).
The wetland habitat within the San Bernardino National Wildlife
Refuge has been adversely affected by undocumented immigration. It is
estimated that approximately 1,000 undocumented immigrants per month
use these important wetlands for bathing, drinking, and other uses
during their journey northward. These activities can contaminate the
water quality of the wetlands and lead to reductions in the prey base
for the northern Mexican gartersnake, as well as increase exposure of
the snake to humans, and thereby increase direct mortality rates (Rosen
and Schwalbe 1988, p. 43; Ernst and Zug 1996, p. 75; Green 1997, pp.
285-286; Nowak and Santana-Bendix 2002, p. 39; Segee and Neeley 2006,
pp. 21-22). In addition, numerous observations of littering and
destruction of vegetation and wildlife occur annually throughout the
San Bernardino National Wildlife Refuge, which adversely affect the
quality and quantity of vegetation as habitat for the northern Mexican
gartersnake (USFWS 2006, p. 95).
There remains the possibility that adverse effects to riparian
communities may increase in the future as land access and
infrastructure restrictions in sensitive wildlife areas may be relaxed
according to proposed policy changes that aim to boost border
enforcement activities in these currently roadless areas and as
concentrated enforcement efforts in urban locations funnel more
undocumented immigrant traffic to remote wilderness areas (Segee and
Neeley 2006, pp. 15-16).
Habitat Threats in Mexico. Threats to northern Mexican gartersnake
habitat in Mexico include the intentional and unintentional
introductions of nonnative species, improper livestock grazing,
urbanization and development, water diversions and groundwater pumping,
loss of vegetation cover and deforestation, erosion, and pollution, as
well as impoundments and dams that have modified or destroyed riparian
and aquatic communities within Mexico in areas where the species
occurred historically (Conant 1974, p. 471; Contreras Balderas and
Lozano 1994, p. 384; va Landa et al. 1997, p. 316; Miller et al. 2005,
pp. 60-61; Abarca 2006). We experienced difficulty finding specific
information documenting that populations of northern Mexican
gartersnakes in Mexico are directly affected by these threats which is
problematic in a rangewide analysis given that approximately 70 to 80
percent of the historic distribution of the northern Mexican
gartersnake occurs in Mexico. We did, however, find enough information
to provide some refined discussion of smaller geographic areas within
Mexico, and acknowledge that many of the threats that affect the
northern Mexican gartersnake in the United States also occur in Mexico
and could affect the northern Mexican gartersnake in similar ways but
at potentially varying intensities.
Conant (2003, p. 4) noted anthropogenic threats to seven
fragmented, endemic subspecies of Mexican gartersnake in the
Transvolcanic Belt Region of southern Mexico, which extends from
southern Jalisco eastward through the state of M[eacute]xico to central
Veracruz which comprises a small proportion of the subspecies' range.
Although Conant (2003) addresses threats to a small percentage of the
historic distribution, many of these rural land uses are regionally
ubiquitous and therefore these threats can be extrapolated to the
surrounding vicinity of the distribution of these seven recently
described subspecies of the Mexican gartersnake in Mexico. Some of
these threats included water diversions, pollution (e.g., discharge of
raw sewage), sedimentation of aquatic habitats, and eutrophication
(increase of dissolved nutrients and decrease of dissolved oxygen) of
lentic (still water) habitats. Conant (2003, p. 4) expressed great
concern that while many of these threats were evident during his field
work in the 1960s, they are ``continuing with increased velocity.''
Water pollution, dams, groundwater pumping, and impoundments were
identified by Miller et al. (2005, pp. 60-61) as significant threats to
aquatic
[[Page 56244]]
biota. 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
[where the northern Mexican gartersnake is distributed]
such as the
R[iacute]o Grande de Santiago below Guadalajara (Jalisco) and
R[iacute]o Colorado downstream of Hoover (Boulder) Dam, have simply
been destroyed by pollution and river alteration.'' Near
Torre[oacute]n, Coahuila, where the northern Mexican gartersnake was
historically distributed, groundwater pumping has resulted in flow
reversal, which has driedup many local springs, drawn arsenicladen
water, further contaminated the area, and resulted in adverse human
health effects in that area. Severe water pollution from untreated
domestic waste is evident downstream of large Mexican cities, and
inorganic pollution from nearby industrialized areas and agricultural
irrigation return flow has dramatically affected aquatic communities
(Miller et al. 2005, p. 60). Miller et al. (2005, p. 61) provides an
excerpt from Soto Galera et al. (1999) addressing the threats to the
R[iacute]o Lerma (Mexico's longest river) where the northern Mexican
gartersnake was historically distributed: ``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.''
Several rivers within the historic distribution of the northern
Mexican gartersnake have been impounded and dammed throughout Mexico,
resulting in habitat modification and the dispersal and establishment
of nonnative species. The damming and modification of the Rio Colorado,
where the northern Mexican gartersnake was distributed, has facilitated
the replacement of the entire native fishery with nonnative species
(Miller et al. 2005, p. 61). Nonnative species continue to pose
significant threats in the decline of native, often endemic, prey
species of the northern Mexican gartersnake in several regions of
Mexico, as discussed further in Factor C below (Miller et al. 2005, p. 60).
Miller et al. (2005) does provide some locality specific
information on the status and threats of freshwater fishes and riparian
and aquatic communities in specific waterbodies throughout Mexico that
historically overlapped, or are adjacent to, the historic distribution
of the northern Mexican gartersnake: the R[iacute]o Grande (dam
construction, p. 78); the Rio Bravo (extirpations, pp. 82, 112);
headwaters of the Rio Lerma (extinction/rediscovery, nonnatives,
pollution, dewatering, pp. 60, 105, 197); Lago de Chapala and its
outlet to the Rio Grande de Santiago (major declines, p. 106); medium-
sized streams throughout the Sierra Madre Occidental (localized
extirpations, logging, dewatering, pp. 109, 177, 247); the Rio Conchos
(extirpations, p. 112); the rios Casas Grandes, Santa Maria, del
Carmen, and Laguna Bustillos (diversions, groundwater pumping,
channelization, flood control practices, pollution, and introduction of
nonnative species, pp. 124, 197); the Rio Santa Cruz (extirpations, p.
140); the Rio Yaqui (nonnatives, pp. 148, Plate 61); the Rio Colorado
(nonnatives, p. 153); the rios Fuerte and Culiacan (logging, p. 177);
canals, ponds, lakes in the endorheic (closed) Valle de Mexico
(nonnatives, extirpations, pollution, pp. 197, 281); the Rio Verde
Basin (dewatering, nonnatives, extirpations, Plate 88); the Rio Mayo
(dewatering, nonnatives, p. 247); the Rio Papaloapan (pollution, p.
252); lagos de Zacapu and Yuriria (habitat destruction, p. 282); and
the Rio Panuco Basin (nonnatives, p. 295).
Conant (1974, pp. 486-489) described significant threats to
northern Mexican gartersnake habitat within its historical distribution
in various locations in western Chihuahua, Mexico, and within the Rio
Concho system where it is known to occur. These threats specifically
included impoundments, diversions, and purposeful introductions of
largemouth bass, common carp, and bullfrogs. We discuss the threats
from nonnative species introductions below in our discussion of Factor
C. McCranie and Wilson (1987, p. 2) discuss threats to the pine-oak
communities of higher elevation habitats in the Sierra Madre
Occidental, 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, especially if the road is paved as
has been the case with (Mexican) Highway 40 through southern Durango.
We feel fortunate to have worked in an area of this country of rapid
population growth that is all too fast disappearing.'' In Mexico, as
compared to the United States, there is believed to be a delay in the
magnitude and significance of adverse effects to riparian communities,
but it is believed that threats to riparian and aquatic communities
that have been observed in Arizona as described below are currently
occurring with increasing significance in several regions across Mexico
within the historic distribution of the northern Mexican gartersnake
(Conant 1974, pp. 471, 487-489; Contreras Balderas and Lozano 1994, pp.
379-381; va Landa et al. 1997, p. 316; Miller et al. 2005, p. 60-61;
Abarca 2006; Rosen 2006).
Collectively, the impacts described above are expected to continue
as a result of Mexico's expanding role as an economical labor force for
international manufacturing under the North American Free Trade
Agreement (NAFTA) and the subsequent increase in population size,
economic growth and development, and infrastructure. Mexico's human
population grew 700 percent from 1910 to 2000 (Miller et al. 2005, p.
60). More recently, Mexico's population increased by 245 percent from
1950 to 2002, and is projected to grow by another 28 percent by 2025
(EarthTrends 2005). As of 1992, Mexico had the second highest gross
domestic product in Latin America at 5.8 percent, following Brazil
(DeGregorio 1992, p. 60). As a result of NAFTA, the number of
maquiladoras (export assembly plants) is expected to increase by as
many as 3,000 to 4,000 (Contreras Balderas and Lozano 1994, p. 384). To
accommodate Mexico's increasing population, rural areas are largely
devoted to food production based on traditional methods, which has led
to serious losses in vegetative cover and soil erosion (va Landa et al.
1997, p. 316). To increase forage and stocking rates for livestock
production in the arid lowlands of northern Mexico, African buffelgrass
(Pennisetum ciliare) was widely introduced in Mexico and has spread on
its own (Burquez-Montijo et al. 2002, p. 131). Buffelgrass invasions
pose a serious threat to native arid ecosystems because buffelgrass
prevents germination of native species, competes for water, crowds out
native vegetation, and creates fine fuels in vegetation communities not
adapted to fire; in such native arid ecosystems, buffelgrass has caused
many changes, including severe soil erosion (Burquez-Montijo et al.
2002, pp. 135, 138). Erosion affects the suitability of habitat for
northern Mexican gartersnakes and their prey species. Recent estimates
indicate that 80 percent of Mexico is affected by soil
[[Page 56245]]
erosion with the most serious erosion occurring in the states of
Guanajuato (43 percent of the state's land area), Jalisco (25 percent
of the state's land area), and Mexico (25 percent of the state's land
area) (va Landa et al. 1997, p. 317), the states in which the northern
Mexican gartersnake historically occurred.
The threats to riparian and aquatic communities in Mexico (such as
the intentional and unintentional introductions of nonnative species,
improper livestock grazing, urbanization and development, water
diversions and groundwater pumping, loss of vegetation cover and
deforestation, erosion, pollution, impoundments, and dams) vary in
their significance both geographically and ecologically, based on
geographical distribution of land management activities and urban
centers, but are expected to continue into the future. Threats that
affect the amount of water within an occupied area directly affect its
suitability to northern Mexican gartersnakes. Threats that alter the
vegetation of occupied habitat reduce the habitat's suitability as
cover for protection from predators, as a foraging area, and as an
effective thermoregulatory site. Nonnative species, explained further
in our Factor C discussion, compete with the northern Mexican
gartersnake for prey as well as prey on juvenile and sub-adult northern
Mexican gartersnakes, which hampers the recruitment of young snakes
into the population and lessens the viability of that population over
time. However, because specific and direct survey information is
significantly limited concerning the presence and potential effect of
these threats to the subspecies in Mexico, this discussion is based on
extrapolation of how we understand these threats to affect the
subspecies in the United States. Furthermore, the subspecies was
historically distributed in several regions within Mexico that have
remained roadless and isolated, thus suggesting that the severity of
threats may be less than that found within the range in United States
where lands have greater past and current economic pressures such as
grazing and development. As such we can not conclude that the
subspecies is likely to become endangered throughout its range in
Mexico. Although we acknowledge that these threats are affecting the
subpecies in the United States, we have determined that the portion of
the subspecies' range in the United States does not constitute a
significant portion of the range of the subspecies or a DPS. Therefore,
on the basis of the best available information, we determine that it is
not likely that the northern Mexican gartersnake will become an
endangered species within the foreseeable future based on threats under
this factor.
B. Overutilization for commercial, recreational, scientific, or
educational purposes
The northern Mexican gartersnake may not be collected in the United
States without special authorization by the Arizona Game and Fish
Department or the New Mexico Department of Game and Fish. We have found
no evidence that current or historical levels of lawful or unlawful
field collecting of northern Mexican gartersnakes has played a
significant role in the decline of this species. The Arizona Game and
Fish Department recently produced field identification cards for
distribution that provide information to assist with the field
identification of each of Arizona's five native gartersnake species as
well as guidance on submitting photo vouchers for university museum
collections. Additionally, universities such as Arizona State
University and the University of Arizona recently began to accept photo
voucher record, versus physical specimens, in their respective museum
collections. We believe these measures further reduce the necessity for
field biologists to collect physical specimens (unless discovered
postmortem) for locality voucher purposes and therefore further reduce
impacts to vulnerable populations from formal biological field
investigations and field specimen collections. We were unable to obtain
any information about the effect of overutilization for commercial,
recreational, scientific, or educational purposes in Mexico.
Specific discussion of the regulatory protections for the northern
Mexican gartersnake is provided under Factor D ``Inadequacy of Existing
Regulatory Mechanisms'' below.
C. Disease or Predation
Disease
Disease in northern Mexican gartersnakes has not yet been
documented as a specific threat in the United States or Mexico.
However, because little is known about disease in wild snakes, it is
premature to conclude that there is no disease threat that could
directly affect remaining northern Mexican gartersnake populations
(Rosen 2006).
Disease and nonnative parasites have been implicated in the decline
in the prey base of the northern Mexican gartersnake. The outbreak of
chytrid fungus (of the genus Batrachochytrium) has been identified as a
chief causative agent in the significant declines of many of the native
ranid frogs and other amphibian species, and regional concerns exist
for the native fish community due to nonnative parasites such as the
Asian tapeworm (Bothriocephalus achelognathi) 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). The chytrid fungus 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 the chytrid fungus a serious threat to
amphibian diversity. In Arizona, chytrid infections have been reported
in several northern Mexican gartersnake native prey species (Morell
1999, pp. 731-732; Sredl and Caldwell 2000, p. 1; Hale 2001, pp. 32-37;
Bradley et al. 2002, p. 207; USFWS 2002a, pp. 40802-40804). Declines of
native prey species of the northern Mexican gartersnake from chytrid
infections have contributed to the decline of this species in the
United States. However, we do not have specific information regarding
potential impacts of chytrid infections on northern Mexican gartersnake
native prey species in Mexico.
We also note that in a pure culture (uncontaminated growth medium),
the fungus Batrachochytrium can grow on boiled snakeskin (keratin),
which indicates the potential for the fungus to live saprobically
(obtaining nutrients from non-living organic matter, commonly dead and
decaying plant or animal matter, by absorbing soluble organic
compounds) on gartersnake skin in the wild if other components of the
ecosystem limit the growth of competing bacteria and oomycetes (a
taxonomic group of fungi that produce oospores such as the genera
Pythium, Phytophthora, and Aphanomyces) (Longcore et al. 1999, p. 227).
While the genus Batrachochytrium has been grown on snakeskin in the
laboratory, no reports of the organism on reptilian hosts in the wild
have been documented. We anticipate diligence in monitoring the status
of incidence of this disease in this species in the wild for early
detection purposes should this potential threat come to fruition in
wild populations of northern Mexican gartersnakes.
Nonnative Species Interactions
A host of native predators prey upon northern Mexican gartersnakes
[[Page 56246]]
including birds of prey, other snakes [kingsnakes (Lampropeltis sp.),
whipsnakes (Masticophis sp.), etc.], wading birds, raccoons (Procyon
lotor), skunks (Mephitis sp.), and coyotes (Canis latrans) (Rosen and
Schwalbe 1988, p. 18). However, nonnative species, such as the
bullfrog, the northern (virile) (Orconectes virilis) and red swamp
(Procambarus clarki) crayfish, and numerous species of exotic sport and
bait fish species continue to be the most prominent threat to the
northern Mexican gartersnake and to its prey base from direct
predation, competition, and modification of habitat in the United
States and potentially in Mexico (Conant 1974, pp. 471, 487-489; Meffe
1985, pp. 179-185; Rosen and Schwalbe 1988, pp. 28, 32; 1997, p. 1;
Bestgen and Propst 1989, pp. 409-410; Clarkson and Rorabaugh 1989, pp.
531, 535; Marsh and Minckley 1990, p. 265; Stefferud and Stefferud
1994, p. 364; Rosen et al. 1995, pp. 257-258; 1996b, pp. 2, 11-13;
2001, p. 2; Degenhardt et al. 1996, p. 319; Fernandez and Rosen 1996,
pp. 8, 23-27; Weedman and Young 1997, pp. 1, Appendices B, C; Inman et
al. 1998, p. 17; Rinne et al. 1998, pp. 4-6; Fagan et al. 2005, pp. 34,
34-41; Olden and Poff 2005, pp. 82-87; Unmack and Fagan 2004, p. 233;
Miller et al. 2005, pp. 60-61; Abarca 2006; Brennan and Holycross 2006,
p. 123; Holycross et al. 2006, pp. 13-15; Rosen and Melendez 2006, p. 54).
Nonnative Species Interactions in the United States. Nonnative
species represent serious threats to the northern Mexican gartersnake
through competition for prey, direct predation, and alteration of
habitat. Riparian and aquatic communities have been dramatically
impacted by a shift in species' composition. Specifically, riparian and
wetland communities have experienced a shift from being historically
dominated by native fauna to being increasingly occupied by an
expanding assemblage of nonnative plant and animal species that have
been intentionally or accidentally introduced, or have colonized new
areas from neighboring occupied localities. For example, nonnative
shrub species in the genus Tamarix have been widely introduced
throughout the western States and appear to thrive in regulated river
systems (Stromberg and Chew 2002, pp. 210-213). Tamarix invasions may
result in habitat alteration from potential effects to water tables,
changes to canopy and ground vegetation structures, and increased fire
risk, which hasten the demise of native cottonwood and willow
communities and affect the suitability of the vegetation component to
northern Mexican gartersnake habitat (Stromberg and Chew 2002, pp. 211-
212; USFWS 2002b, p. H-9).
Declines in the Northern Mexican Gartersnake Anuran Prey Base in
the United States. The decline of the northern Mexican gartersnake
within its historical and extant distribution was subsequent to the
declines in its prey base (native amphibian and fish populations) from
introductions of nonnative bullfrogs, crayfish, and numerous species of
exotic sport and bait fish as documented in an extensive body of
literature (Nickerson and Mays 1970, p. 495; Hulse 1973, p. 278; Vitt
and Ohmart 1978, p. 44; Meffe 1985, pp. 179-185; Ohmart et al. 1988,
pp. 143-147; Rosen and Schwalbe 1988, pp. 28-31; 1997, pp. 8-16;
Bestgen and Propst 1989, pp. 409-410; Clarkson and Rorabaugh 1989, pp.
531-538; Marsh and Minckley 1990, p. 265; Sublette et al. 1990, pp.
112, 243, 246, 304, 313, 318; Stefferud and Stefferud 1994, p. 364;
Holm and Lowe 1995, p. 5; Rosen et al. 1995, pp. 251, 257-258; 1996a,
pp. 2-3; 1996b, p. 2; 2001, p. 2; Sredl et al. 1995a, pp. 7-8; 1995b,
pp. 8-9; 1995c, pp. 7-8; 2000, p. 10; Degenhardt et al. 1996, p. 319;
Fernandez and Rosen 1996, pp. 8-27; Drost and Nowak 1997, p. 11;
Weedman and Young 1997, pp. 1, Appendices B, C; Inman et al. 1998, p.
17; Rinne et al. 1998, pp. 4-6; Turner et al. 1999, p. 11; Nowak and
Spille 2001, p. 11; Bonar et al. 2004, p. 3; Fagan et al. 2005, pp. 34,
34-41; Olden and Poff 2005, pp. 82-87; Holycross et al. 2006, pp. 13-
15, 52-61; Brennan and Holycross 2006, p. 123). The northern Mexican
gartersnake is particularly vulnerable to a loss in native prey species
(Rosen and Schwalbe 1988, p. 20). Rosen et al. (2001, pp. 10, 13, 19)
examined this issue in detail and proposed a hypothesis involving two
reasons for the decline in northern Mexican gartersnakes following the
loss or decline in the native prey base: (1) The northern Mexican
gartersnake is unlikely to increase foraging efforts at the risk of
increased predation; and (2) the species needs substantial food
regularly to maintain its weight and health. If forced to forage more
often for smaller prey items, a reduction in growth and reproductive
rates will result (Rosen et al. 2001, pp. 10, 13).
Native ranid frog species such as lowland leopard frogs, northern
leopard frogs, and federally threatened Chiricahua leopard frogs have
all experienced significant declines 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
will be extirpated from 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.
Declines in the native leopard frog populations in Arizona have
significantly contributed to declines in the northern Mexican
gartersnake, as a primary native predator. Scotia Canyon in the
Huachuca Mountains of southeastern Arizona is a location where
corresponding declines between leopard frog and northern Mexican
gartersnake populations has 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 in low numbers
were observed in decline during the early 1980s with low capture rates
remaining through the early 1990s (Holm and Lowe 1995, pp. 27-35).
Surveys documented further decline in 2000 (Rosen et al. 2001, pp. 15-
16). A former stronghold for the northern Mexican gartersnake, the San
Bernardino National Wildlife Refuge has also been affected by
correlative declines between leopard frog and northern Mexican
gartersnake populations (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). Declines of leopard frog
populations, often correlated with nonnative species introductions (but
also with the spread of chytridiomycosis, symptomatic disease caused by
the chytrid fungus, and habitat modification and destruction), has not
just occurred throughout southeastern Arizona, but throughout much of
the U.S. distribution of the northern Mexican gartersnake based on
survey data (Nickerson and Mays 1970, p. 495; Vitt and Ohmart 1978, p.
44; Ohmart et al. 1988, p. 150; Rosen and Schwalbe 1988,
[[Page 56247]]
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) recently
documented 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
watershed) in the vicinity of the Forest Service Cabin, at the Page
Springs and Bubbling Ponds fish hatchery along Oak Creek, Sycamore
Creek (Verde River watershed) 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.''
Rosen et al. (2001, p. 22) concluded that the presence and
expansion of nonnative predators (mainly bullfrogs, crayfish, and green
sunfish) are the primary causes of decline in northern Mexican
gartersnakes in southeastern Arizona. Specifically, the authors
identified the expansion of bullfrogs into the Sonoita grasslands (the
threshold to the Canelo Hills) and the introduction of crayfish into
Lewis Springs as being of particular concern in terms of future
recovery efforts for the northern Mexican gartersnake. It should also
be noted that Rosen et al. (2001, Appendix I) documented the decline of
several native fish species in several locations visited, further
affecting the prey base of northern Mexican gartersnakes. Rosen et al.
(1995, pp. 252-253) sampled 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 ectothermic aquatic and
semi-aquatic vertebrate species detected were nonnative. The most
commonly encountered nonnative species was the bullfrog (Rosen et al.
1995, p. 254).
Declines in the Northern Mexican Gartersnake Native Fish Prey Base
in the United States. Native fish species such as the federally
endangered Gila chub, petitioned roundtail chub, and federally
endangered Gila topminnow are among the primary prey species for the
northern Mexican gartersnake (Rosen and Schwalbe 1988, p. 18). Similar
to bullfrogs, predatory nonnative fish species such as largemouth bass
also prey upon juvenile northern Mexican gartersnakes. Additionally
both nonnative sport and bait compete with the northern Mexican
gartersnake in terms of its native fish and native anuran prey base.
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 gartersnakes). Holycross et al. (2006, pp. 53-55) recently
documented significantly depressed or extirpated native fish prey bases
for the northern Mexican gartersnake along the Agua Fria in the
vicinity of Table Mesa Road and the Little Grand Canyon Ranch, along
Dry Creek from Dugas Road to Little Ash Creek, along Little Ash Creek
from Brown Spring to Dry Creek, along Sycamore Creek (Agua Fria
watershed) in the vicinity of the Forest Service Cabin, and along
Sycamore Creek (Verde River watershed) in the vicinity of its
confluence with the Verde River north of Clarkdale.
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 whose
historical ranges overlap with the historical distribution of the
northern Mexican gartersnake. These native fish species were likely
prey species for the northern Mexican gartersnake, including: 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, 51 FR 23769, July 1,
1986), loach minnow (Tiaroga cobitis, 51 FR 39468, October 28, 1986),
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 occidentalis, 32 FR 4001,
March 11, 1967)]. In total within Arizona, 19 of 31 (61 percent) of
native fish species are listed under the Act. Arizona ranks the highest
of all 50 States in the percentage of native fish species at risk (85.7
percent, Stein 2002, p. 21).
Fragmentation of extant listed native fish populations is
exacerbating the decline of these species and may preclude their
recovery as well as continue to affect their role in the prey base of
northern Mexican gartersnakes. Fagan et al. (2005, pp. 34-41) examined
the correlation between fragmentation of extant distributions and the
relative risk of extinction of any given species. They found the
strongest correlation to risk of extinction due to fragmentation of
fish populations occurred at the intermediate to large spatial scales,
which geographically correspond to tributaries and river basins (Fagan
et al. 2005, p. 38). At this range in spatial scale, the effects of dam
building, water diversions, and introduced nonnatives appear to be
significant factors exacerbating the fragmentation by acting as
barriers to the exchange of genetic material among listed fish
populations (Fagan et al. 2005, pp. 38-39).
Olden and Poff (2005, p. 75) stated that environmental degradation
and the proliferation of nonnative fish species threaten the endemic
and unique fish faunas of the American Southwest. The fastest expanding
nonnative species are red shiner (Cyprinella lutrensis), fathead minnow
(Pimephales promelas), green sunfish (Lepomis cyanellus), 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 dolomieue), have been introduced into formerly and
currently occupied northern Mexican gartersnake habitat (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; Voeltz 2002, p. 88; Bonar et al. 2004, pp. 1-108).
[[Page 56248]]
Several authors have identified both the presence of nonnative fish
species as well as their deleterious effects on native species within
Arizona. 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 influence in
the lower reaches where the northern Mexican gartersnake is considered
extant. At the Gisela sampling point, four of six sampling attempts
resulted in no fish captured; of the 41 fish captured in the remaining
two attempts, 90 percent were nonnative, including 28 fathead minnows,
5 green sunfish, 3 red shiner, and 1 yellow bullhead. 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 roundtail chub
populations (Voeltz 2002, p. 40).
A report provided by Bonar et al. (2004, pp. 1-108) is the most
current and perhaps one of the most complete assessments of native and
nonnative fish species interactions in the Verde River mainstem.
Overall, Bonar et al. (2004, p. 57) found that nonnative fishes were
approximately 2.6 times more dense per unit volume of river than native
fishes, and their standing crop was approximately 2.8 times that of
native fishes per unit volume of river. Bonar et al. (2004, p. 79)
verified the findings of Voeltz (2002, pp. 71, 88), in stating that red
shiner were the most commonly encountered nonnative fish species in the
Verde River by almost four-fold; they found the species to be present
throughout the Verde River year-around, but noted the highest numbers
in the reach between Beasley Flat to Sheep Bridge above Horseshoe
Reservoir in riffle habitats. River reaches above Horseshoe Reservoir
have resident self-sustaining populations of bass, green sunfish,
catfish, and carp, with a low, unstable native fish community, which
results in fewer native fish predation observations in sampling results
for this reach (Bonar et al. 2004, pp. 80, 87). Reaches below Bartlett
Reservoir had both high native and nonnative fish abundance, which
resulted in more frequent observations of nonnative predation on native
fish according to Bonar et al. (2004, p. 87). Lastly, Bonar et al.
(2004, p. 6) found that channel and flathead catfish, green sunfish,
largemouth and smallmouth bass, and yellow bullhead had the highest
rates of piscivory (fish predation) on native and nonnative fish
species in all river reaches; of these species, largemouth bass were
documented as the most significant predator on native fish.
Northern Mexican gartersnakes can successfully use some nonnative
species, such as mosquitofish and red shiner, as prey species. However,
all other nonnative species, most notably the spiny-rayed fish, are not
considered prey species for the northern Mexican gartersnake. These
nonnative species can be difficult to swallow due to their body shape
and spiny dorsal fins, are predatory on juvenile gartersnakes, and
reduce the abundance of or completely eliminate native fish
populations. This is particularly important in the wake of a stochastic
event such as flooding, extreme water temperatures, or excessive
turbidity. Native fish are adapted to the dramatic fluctuations in
water conditions and flow regimes and persist in the wake of stochastic
events as a prey base for the northern Mexican gartersnake. Nonnative
fish, even species that may be used as prey by the northern Mexican
gartersnake, generally are ill-adapted to these conditions and may be
removed from the area temporarily or permanently, depending on the
hydrologic connectivity to extant populations. If an area is solely
comprised of nonnative fish, the northern Mexican gartersnake may be
faced with nutritional stress or starvation. The most conclusive
evidence for the northern Mexican gartersnake's intolerance for
nonnative fish remains in the fact that, in most incidences, nonnative
fish species generally do not occur in the same locations as the
northern Mexican gartersnake and its native prey species.
Bullfrog Diet and Distribution in the United States. Bullfrogs are
widely considered one of the most serious threats to the northern
Mexican gartersnake throughout its range (Conant 1974, pp. 471, 487-
489; Rosen and Schwalbe 1988, pp. 28-30; Rosen et al. 2001, pp. 21-22).
Bullfrogs adversely affect northern Mexican gartersnakes through direct
predation of juvenile and sub-adults and from competition with native
prey species. Bullfrogs first appeared in Arizona in 1926, as a result
of a systematic introduction effort by the State Game Department (now,
the Arizona Game and Fish Department) for the purposes of sport hunting
and as a food source. (Tellman 2002, p. 43). By 1982, the Arizona Game
and Fish Department had systematically introduced some 682,000 bullfrog
tadpoles into streams throughout the State (Tellman 2002, p. 43).
Bullfrogs are extremely prolific, adept at colonizing new areas, and
may disperse to distances of 6.8 miles (10.9 km) and likely further
within drainages (Bautista 2002, p. 131; Rosen and Schwalbe 2002a, p.
7; Casper and Hendricks 2005, p. 582). Batista (2002, p. 131) confirmed
``the strong colonizing skills of the bullfrog and that the
introduction of this exotic species can disturb local anuran communities.''
Bullfrogs are voracious, opportunistic, even cannibalistic
predators that readily attempt to consume any animal smaller than
themselves, including conspecifics (other species within the same
genus) which can encompass 80 percent of their diet (Casper and
Hendricks 2005, p. 543). Bullfrogs have demonstrated astonishing
variability in their diet, which has been documented to include
vegetation, earthworms, leeches, insects, centipedes, millipedes,
spiders, scorpions, crayfish, snails, numerous species of larval and
metamorphosed amphibians, fish, small alligators, turtles, lizards,
numerous species of snakes [seven genera; including six different
species of gartersnakes, two species of rattlesnakes, and Sonoran
gophersnakes (Pituophis catenifer affinis)], small mammals (e.g.,
chipmunks, cotton rats, shrews, mice, and voles), numerous species of
birds, bats, muskrats, and even juvenile mink (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, p. 544; Combs et al. 2005, p.
439; Wilcox 2005, p. 306).
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 watershed, 62 percent of sites in the
Verde River watershed, 25 percent of sites in the Salt River watershed,
and 22 percent of sites in the Gila River watershed. 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 documented the presence of bullfrogs
through their survey efforts Statewide in specific regional areas,
drainages, and disassociated wetlands that include the Kaibab National
Forest (Sredl et al. 1995a, p. 7); the Coconino National Forest (Sredl
et al. 1995c, p. 7); the White Mountain Apache Reservation (Hulse 1973,
p. 278); Beaver Creek (tributary to the Verde River) (Drost and Nowak
1997, p. 11); the Watson Woods Riparian Preserve near Prescott (Nowak
and Spille 2001, p. 11); the Tonto National Forest (Sredl et al. 1995b,
p. 9);
[[Page 56249]]
the Lower Colorado River (Vitt and Ohmart 1978, p. 44; Clarkson and
DeVos 1986, pp. 42-49; Ohmart et al. 1988, p. 143); the Huachuca
Mountains (Rosen and Schwalbe 1988, Appendix I; Holm and Lowe 1995, pp.
27-35; Sredl et al. 2000, p. 10; Rosen et al. 2001, Appendix I); the
Pinaleno Mountains region (Nickerson and Mays 1970, p. 495); the San
Bernardino National Wildlife Refuge (Rosen and Schwalbe 1988, Appendix
I; 1995, p. 452; 1996, pp. 1-3; 1997, p. 1; 2002b, pp. 223-227; 2002c,
pp. 31, 70; Rosen et al. 1995, p. 254; 1996b, pp. 8-9; 2001, Appendix
I); the Buenos Aires National Wildlife Refuge (Rosen and Schwalbe 1988,
Appendix I); the Arivaca Area (Rosen and Schwalbe 1988, Appendix I;
Rosen et al. 2001, Appendix I); Cienega Creek drainage (Rosen et al.
2001, Appendix I); Babocamari River drainage (Rosen et al. 2001,
Appendix I); Turkey Creek drainage (Rosen et al. 2001, Appendix I);
O'Donnell Creek drainage (Rosen et al. 2001, Appendix I); Audubon
Research Ranch near Elgin (Rosen et al. 2001, Appendix I); Santa Cruz
River drainage (Rosen and Schwalbe 1988, Appendix I; Rosen et al. 2001,
Appendix I); San Rafael Valley (Rosen et al. 2001, Appendix I); San
Pedro River drainage (Rosen and Schwalbe 1988, Appendix I; Rosen et al.
2001, Appendix I); Bingham Cienega (Rosen et al. 2001, Appendix I);
Sulfur Springs Valley (Rosen et al. 1996a, pp. 16-17); Whetstone
Mountains region (Turner et al. 1999, p. 11); Aqua Fria River drainage
(Rosen and Schwalbe 1988, Appendix I; Holycross et al. 2006, pp. 13,
15-18, 52-53); Verde River drainage (Rosen and Schwalbe 1988, Appendix
I; Holycross et al. 2006, pp. 13, 26-28, 55-56); greater metropolitan
Phoenix area (Rosen and Schwalbe 1988, Appendix I); greater
metropolitan Tucson area (Rosen and Schwalbe 1988, Appendix I); Sonoita
Creek drainage (Rosen and Schwalbe 1988, Appendix I); Sonoita
Grasslands (Rosen and Schwalbe 1988, Appendix I); Canelo Hills (Rosen
and Schwalbe 1988, Appendix I); Pajarito Mountains (pers. observation,
J. Servoss, Fish and Wildlife Biologist, U.S. Fish and Wildlife
Service); Picacho Reservoir (Rosen and Schwalbe 1988, Appendix I); Dry
Creek drainage (Holycross et al. 2006, pp. 19, 53); Little Ash Creek
drainage (Holycross et al. 2006, pp. 19, 54); Oak Creek drainage
(Holycross et al. 2006, pp. 23, 54); Sycamore Creek drainages
(Holycross et al. 2006, pp. 20, 25, 54-55); Rye Creek drainage
(Holycross et al. 2006, pp. 37, 58); Spring Creek drainage (Holycross
et al. 2006, pp. 25, 59); Tonto Creek drainage (Holycross et al. 2006,
pp. 40-44, 59); San Francisco River drainage (Holycross et al. 2006,
pp. 49-50, 61); and the upper Gila River drainage (Holycross et al.
2006, pp. 45-50, 60-61).
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 San Bernardino National
Wildlife Refuge in addition to a control site with no bullfrog removal
in similar habitat on the Buenos Aires National Wildlife Refuge.
Removal of adult bullfrogs resulted in a substantial increase in
younger age-class bullfrogs where removal efforts were the most
intensive (Rosen and Schwalbe 1997, p. 6). 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 (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). Consequently, this strategy was viewed as
being potentially ``self-defeating'' and ``counter-productive'' but
required further investigation (Rosen and Schwalbe 1997, p. 6).
Bullfrog Effects on the Native Anuran Prey Base for the Northern
Mexican Gartersnake in the United States. Bullfrog introductions in the
United States and Mexico have adversely affected the native leopard
frog prey base for northern Mexican gartersnakes (Conant 1974, pp. 471,
487-489; Hayes and Jennings 1986, pp. 491-492; Rosen and Schwalbe 1988,
p. 28-30; 2002b, pp. 232-238; Rosen et al. 1995, pp. 257-258; 2001, pp.
2, Appendix I). Different age classes of bullfrogs within a community
can affect native ranid populations via different mechanisms. Juvenile
bullfrogs may affect native ranids by competition, male bullfrogs may
affect native ranids by predation, and female bullfrogs may affect
native ranids by 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 on microhabitat use, but also suggested that an
individual ranid frog species' physical ability to escape influences
the effect of bullfrogs on each native ranid community.
Kupferberg (1994, p. 95) found that where bullfrogs were present in
California, native anurans were rare or absent. Effects of larval
bullfrogs on native ranid frogs have also been described in the
literature. Survivorship of larval threatened California red-legged
frogs (Rana aurora) was 700 percent greater in the absence of bullfrog
larvae (Lawler et al. 1999). Bury and Whelan (1986, pp. 9-10)
implicated bullfrog introductions in the decline of several native
ranid frogs in several States within the western United States
including Nevada, California, Montana, Colorado, Oregon, and
Washington. Hayes and Jennings (1986, pp. 500-501) conclude that while
bullfrog introductions have affected the status of native ranid frogs
throughout the western United States, the synergistic effect of other
factors, such as habitat alteration and destruction, introduced
nonnative fishes, commercial exploitation, toxicants, pathogens and
parasites, and acid rain, likely also played significant roles.
Bullfrog Predation on Northern Mexican Gartersnakes in the United
States. Sub-adult and adult bullfrogs not only compete with the
northern Mexican gartersnake for prey items, but directly prey upon
juvenile and occasionally sub-adult northern Mexican 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). 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 neonate (newborn) and juvenile age size classes due
to bullfrogs preying on young small snakes, which ultimately leads to
low recruitment levels (reproduction and survival of young) (Rosen and
Schwalbe 1988, p. 18; Holm and Lowe 1995, p. 34).
The tails of gartersnakes are easily broken-off through predation
attempts (tails of gartersnakes do not regenerate), which may assist in
escaping an individual predation attempt but may also lead to infection
or compromise an individual's physical ability to escape
[[Page 56250]]
future predation attempts or successfully forage. The incidence of tail
breaks in gartersnakes can often be used to assess predation pressures
within gartersnake populations. Rosen and Schwalbe (1988, p. 22) found
the incidence of tail breaks to be statistically higher in females than
in males. Fitch (2003, p. 212) also found that tail breaks in the
common gartersnake occurred more frequently in females than males and
in adults more than in juveniles. Fitch (2003, p. 212) also 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.
Furthermore, Mushinsky and Miller (1993, pp. 662-664) found that the
incidence of tail injury in water snakes in the genera Nerodia and
Regina (which have similar life histories to northern Mexican
gartersnakes) was higher in females than in males and in adults more
than juveniles. We believe this could be explained by higher basking
rates associated with gravid (pregnant) females that increased their
visibility to predators and that predation on juvenile snakes generally
results in complete consumption of the animal, which would limit
observations of tail injury in the juvenile age class. Rosen and
Schwalbe (1988, p. 22) suggested that the indication that female
northern Mexican gartersnakes bear more injuries is consistent with the
inference that they employ a riskier foraging strategy. 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 mortality.
Ecologically significant observations on tail injuries were made by
Rosen and Schwalbe (1988, pp. 28-31) from the once-extant population of
northern Mexican gartersnakes on the San Bernardino National Wildlife
Refuge where 78 percent of specimens had broken tails with a ``soft and
club-like'' terminus, which suggests repeated injury from multiple
predation attempts. While palpating (medically examining by touch)
gravid female northern Mexican gartersnakes, Rosen and Schwalbe (1988,
p. 28) noted bleeding from this region which suggested the snakes
suffered from ``squeeze-type'' injuries inflicted by adult bullfrogs.
While a sub-adult or adult northern Mexican gartersnake may survive an
individual predation attempt from a bullfrog while only incurring tail
damage, secondary effects from infection of the wound can significantly
contribute to mortality of individuals.
Research on the effects of attempted predation performed by
Mushinsky and Miller (1993, pp. 661-664) and Willis et al. (1982, pp.
100-101) supports the observations made by Holm and Lowe (1995, p. 34)
on the northern Mexican gartersnake population age class structure in
Scotia Canyon in the Huachuca Mountains of southeastern Arizona in the
early 1990s. Specifically, Holm and Lowe (1995, pp. 33-34) observed a
conspicuously greater number of adult snakes, in that population than
sub-adult snakes as well as a higher incidence of tail injury (89
percent) in all snakes captured. Bullfrogs have been identified as the
primary cause for both the collapse of the native leopard frog (prey
base for the northern Mexican gartersnake) and northern Mexican
gartersnake populations on the San Bernardino National Wildlife Refuge
(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).
Rosen and Schwalbe (1988, p. 18) stated that the low survivorship of
neonates, and possibly yearlings, due to bullfrog predation is an
important proximate cause of population declines of this snake at the
San Bernardino National Wildlife Refuge and throughout its distribution
in Arizona.
Effects of Crayfish on Northern Mexican Gartersnakes in the United
States. Crayfish represent another category of nonnative species threat
as they are a primary threat to many prey species of the northern
Mexican gartersnake and may also prey upon juvenile gartersnakes
(Fernandez and Rosen 1996, p. 25; Voeltz 2002, pp. 87-88). 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 trophic structures (food
chains) in riparian and aquatic ecosystems through their effect on
vegetative structure, stream substrate 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). Fernandez and Rosen (1996, pp. 6-19, 52-56) and Rosen
(1987, p. 5) discussed observations of inverse relationships between
crayfish abundance and native herpetofauna including narrow-headed
gartersnakes (Thamnophis rufipunctatus rufipunctatus), 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 also prey on fish eggs and larvae (Inman et
al. 1998, p. 17).
Crayfish alter the abundance and structure of aquatic vegetation by
grazing on aquatic and semiaquatic vegetation, which reduces the cover
needed for 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) also found that crayfish
frequently burrow into stream banks, which leads to increased bank
erosion, stream turbidity, and siltation of substrates. Creed (1994, p.
2098) found that filamentous alga (Cladophora glomerata) was at least
10-fold greater in aquatic habitat absent crayfish. Filamentous alga is
an important component of aquatic vegetation that provides cover for
foraging gartersnakes as well as microhabitat for prey species.
Inman et al. (1998, p. 3) documented nonnative crayfish as widely
distributed and locally abundant in a broad array of natural and
artificial lotic (free-flowing) and lentic (still water) habitats
throughout Arizona, many of which overlapped the historical and extant
distribution of the northern Mexican gartersnake. Hyatt (undated, p.
71) concluded that the majority of waters in Arizona contained at least
one species of crayfish. Holycross et al. (2006, p. 14) found crayfish
in 64 percent of the sample sites in the Agua Fria watershed; in 85
percent of the sites in the Verde River watershed; in 46 percent of the
sites in the Salt River watershed; and in 67 percent of the sites in
the Gila River watershed. In total, crayfish were recently observed at
35 (61 percent) of the 57 sites surveyed across the Mogollon Rim
(Holycross et al. 2006, p. 14).
Several other authors have specifically documented the presence of
[[Page 56251]]
crayfish in many areas and drainages throughout Arizona, which is
testament to their ubiquitous distribution in Arizona and their strong
colonizing abilities. These areas included the Kaibab National Forest
(Sredl et al. 1995a, p. 7); the Coconino National Forest (Sredl et al.
1995c, p. 7); the Watson Woods Riparian Preserve near Prescott (Nowak
and Spille 2001, p. 33); the Tonto National Forest (Sredl et al. 1995b,
p. 9); the Lower Colorado River (Ohmart et al. 1988, p. 150; Inman et
al. 1998, Appendix B); the Huachuca Mountains (Sredl et al. 2000, p.
10); the Arivaca Area (Rosen et al. 2001, Appendix I); Babocamari River
drainage (Rosen et al. 2001, Appendix I); O'Donnell Creek drainage
(Rosen et al. 2001, Appendix I); Santa Cruz River drainage (Rosen and
Schwalbe 1988, Appendix I; Rosen et al. 2001, Appendix I); San Pedro
River drainage (Inman et al. 1998, Appendix B; Rosen et al. 2001,
Appendix I); Aqua Fria River drainage (Inman et al. 1998, Appendix B;
Holycross et al. 2006, pp. 14, 15-18, 52-54); Verde River drainage
(Inman et al. 1998, Appendix B; Holycross et al. 2006, pp. 14, 20-28,
54-56); Salt River drainage (Inman et al. 1998, Appendix B; Holycross
et al. 2006, pp. 15, 29-44, 56-60); Black River drainage (Inman et al.
1998, Appendix B); San Francisco River drainage (Inman et al. 1998,
Appendix B; Holycross et al. 2006, pp. 14, 49-50, 61); Nutrioso Creek
drainage (Inman et al. 1998, Appendix B); Little Colorado River
drainage (Inman et al. 1998, Appendix B); Leonard Canyon Drainage
(Inman et al. 1998, Appendix B); East Clear Creek drainage (Inman et
al. 1998, Appendix B); Chevelon Creek drainage (Inman et al. 1998,
Appendix B); Eagle Creek drainage (Inman et al. 1998, Appendix B;
Holycross et al. 2006, pp. 47-48, 60); Bill Williams drainage (Inman et
al. 1998, Appendix B); Sabino Canyon drainage (Inman et al. 1998,
Appendix B); Dry Creek drainage (Holycross et al. 2006, pp. 19, 53);
Little Ash Creek drainage (Holycross et al. 2006, pp. 19, 54); Sycamore
Creek drainage (Holycross et al. 2006, pp. 25, 54-55); East Verde River
drainage (Holycross et al. 2006, pp. 21-22, 54); Oak Creek drainage
(Holycross et al. 2006, pp. 23, 54); Pine Creek drainage (Holycross et
al. 2006, pp. 24, 55); Spring Creek drainage (Holycross et al. 2006,
pp. 25, 55); Big Bonito Creek drainage (Holycross et al. 2006, pp. 29,
56); Cherry Creek drainage (Holycross et al. 2006, pp. 33, 57); East
Fork Black River drainage (Holycross et al. 2006, pp. 34, 57); Haigler
Creek drainage (Holycross et al. 2006, pp. 35, 58); Houston Creek
drainage (Holycross et al. 2006, pp. 35-36, 58); Rye Creek drainage
(Holycross et al. 2006, pp. 37, 58); Tonto Creek drainage (Holycross et
al. 2006, pp. 40-44, 59); Blue River drainage (Holycross et al. 2006,
pp. 45, 60); Campbell Blue River drainage (Holycross et al. 2006, pp.
46, 60); and the Gila River drainage (Inman et al. 1998, Appendix B;
Holycross et al. 2006, pp. 45-50, 61).
Bullfrog and Crayfish Eradication in the United States. As
previously noted, nonnative species such as bullfrogs and crayfish have
proven difficult, if not impossible, to eradicate once established in
certain environments. Bullfrogs, for example, are particularly damaging
to, and persistent in, riparian communities. A population of adult
bullfrogs can sustain itself even when the native vertebrate prey base
has been severely reduced or extirpated because adult bullfrogs are
cannibalistic and larval bullfrogs can be sustained by grazing on
aquatic vegetation (Rosen and Schwalbe 1995, p. 452). Effective removal
of semi-aquatic nonnative species is possible in simple, geographically
isolated systems that can be manipulated (e.g., stock tanks); however,
it can be expensive, and specially designed fencing is likely needed to
prevent reinvasion until entire landscapes (e.g., an entire valley)
have been cleared of nonnative species (Rosen and Schwalbe 2002a, p. 7;
Hyatt undated). No single method is available to effectively remove
bullfrogs or crayfish from lotic, or complex inter-connected systems
(Rosen and Schwalbe 1996a, pp. 5-8; 2002a, p. 7; Hyatt Undated, pp. 63-
71). The inability of land managers to effectively address the invasion
of nonnative species in such communities highlights the serious nature
of nonnative species invasions. Hyatt (undated, p. 71) concluded that
successful eradication of crayfish in Arizona is highly unlikely. While
potential threats to physical habitat from human land use activities
can usually be lessened or removed completely with adjustments to land
management practices, the concern for the apparent irreversibility of
nonnative species invasions becomes paramount which leaves us to
conclude that nonnative species are the greatest threat to the northern
Mexican gartersnake due to the long-term implications.
Nonnative Fish distribution and Community Interactions in the
United States. 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. Rosen et al. (2001,
Appendix I) found nonnative fish in the following survey locations: the
Arivaca Area; Babocamari River drainage; O'Donnell Creek drainage;
Audubon Research Ranch (Post Canyon) near Elgin; Santa Cruz River
drainage; Agua Caliente Canyon; Santa Catalina Mountains; and the San
Pedro River drainage. Holycross et al. (2006, pp. 14-15, 52-61) found
nonnative fish in the Aqua Fria River drainage; the Verde River
drainage; the Dry Creek drainage; the Little Ash Creek drainage; the
Sycamore Creek drainage; the East Verde River drainage; the Oak Creek
drainage; the Pine Creek drainage; the Big Bonito Creek drainage; the
Black River drainage; the Canyon Creek drainage; the Cherry Creek
drainage; the Christopher Creek drainage; the East Fork Black River
drainage; the Haigler Creek drainage; the Houston Creek drainage; the
Rye Creek drainage; the Salt River drainage; the Spring Creek drainage;
the Tonto Creek drainage; the Blue River drainage; the Campbell Blue
River drainage; the Eagle Creek drainage; and the San Francisco River
drainage. Other authors have documented the presence of nonnative fish
through their survey efforts in specific regions that include the Tonto
National Forest (Sredl et al. 1995b, p. 8) and the Huachuca Mountains
(Sredl et al. 2000, p. 10).
Holycross et al. (2006, pp. 14-15) found nonnative fish species
while surveying for narrow-headed and Mexican gartersnakes in 64
percent of the sample sites in the Agua Fria watershed, 85 percent of
the sample sites in the Verde River watershed, 75 percent of the sample
sites in the Salt River watershed, and 56 percent of the sample sites
in the Gila River watershed. 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). While the locations and drainages identified above that
are known to support populations of nonnative fish do not provide a
thorough representation of the status of nonnative fish distribution
Statewide in Arizona, it is well documented that nonnative fish have
infiltrated the majority of aquatic communities in Arizona.
Rinne et al. (1998, p. 3) documented over a dozen species of
nonnative fish that have been stocked within the historical
distribution of the northern Mexican gartersnake in the Verde Basin
with over 850 stocking events occurring
[[Page 56252]]
in Horseshoe and/or Bartlett reservoirs and almost 4,500 in streams
(mostly tributaries to the Verde) over the past 60 years. Rinne et al.
(1998, pp. 4-6) found that in all but the uppermost reach, nonnatives
predominated the sampling results in the Verde River. Voeltz (2002, p.
88) documented an ``alarming trend'' in the Verde River with the
reduction of native fish abundance corresponding with an explosion in
red shiner populations.
Nonnative fish can also affect native amphibian populations.
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 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.
Inversely, gartersnake predation on nonnative species, such as
centrarchids, may physically harm the snake. Choking injuries to
northern Mexican gartersnakes may occur from attempting to ingest
nonnative spiny-rayed fish species (such as green sunfish and bass)
because the spines located in the dorsal fins of these species can
become lodged, or cut into the gut tissue of the snake, as observed in
narrow-headed gartersnakes (Nowak and Santana-Bendix 2002, p. 25).
Nonnative fish invasions can indirectly affect the health,
maintenance, and reproduction of the northern Mexican gartersnake by
altering its foraging strategy and foraging success. Observations made
by Dr. Phil Rosen at Finley Tank on the Audubon Research Ranch near
Elgin, Arizona, of northern Mexican gartersnake populations and
individual growth trends prior to the arrival of the nonnative
bullfrog, provides information on the effects of nonnative fish
invasions and the likely nutritional ramifications of a fish-only diet
in a species that normally has a varied diet largely supported by
amphibian prey items (Rosen et al. 2001, p. 19). The more energy
expended in foraging, coupled by the reduced number of small to medium-
sized fish available in lower densities, may lead to deficiencies in
nutrition affecting growth and reproduction because energy is instead
allocated to maintenance and the increased energy costs of intense
foraging activity (Rosen et al. 2001, p. 19). In contrast, a northern
Mexican gartersnake diet that includes both fish and amphibians such as
leopard frogs provides larger prey items which reduce 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 in juvenile snakes that were deprived of regular
feedings versus the control group that were fed regularly at natural
frequencies. Reduced foraging success may therefore increase mortality
rates in the juvenile size class and consequently affect recruitment of
northern Mexican gartersnakes where their prey base has been
compromised by nonnative species.
Nonnative fish species also facilitate the invasion of other
aquatic nonnative species such as bullfrogs. Adams et al. (2003, pp.
343, 349) found that the invasion of nonnative fish species indirectly
facilitates the invasion of bullfrogs. Survivorship of tadpoles is
increased when nonnative fish prey upon predatory macroinvertebrates,
which reduces the densities of predatory macroinvertebrates and relaxes
their predation rate on bullfrog tadpoles. These findings support the
``invasional meltdown'' hypothesis, which suggests that when positive
interactions among nonnatives are prevalent, that community of
nonnative species can increase the probability of further invasions
(Simberloff and Von Holle 1999, p. 21; Adams et al. 2003, pp. 343, 348-
350). While mutually facilitative interactions among introduced species
have not been thoroughly examined, it has been concluded that
nonnatives can and do facilitate the expansion of other nonnative
species (Simberloff and Van Holle 1999, p. 21).
Nonnative Species in Mexico. The native fish prey base for northern
Mexican gartersnakes has been dramatically affected by the introduction
of nonnative species in several regions of Mexico (Conant 1974, pp.
471, 487-489; Miller et al. 2005, pp. 60-61; Abarca 2006). In the lower
elevations of Mexico where northern Mexican gartersnakes occurred
historically and may still be extant, 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 become extinct
due to human activities (Contreras Balderas and Lozano 1994, pp. 383-
384). In 1979, The American Fisheries Society listed 69 species of
native fish in Mexico as threatened or in danger of becoming extinct.
Ten years later that number rose to 123 species, an increase of 78
percent (Contreras Balderas and Lozano 1994, pp. 383-384). Miller et
al. (2005, p. 60) concludes that some 20 percent of Mexico's native
fish are threatened or in danger of becoming extinct. Nonnative species
are increasing everywhere throughout Mexico and the outlook for this
trend looks ``bleak'' for native fish according to Miller et al. (2005,
p. 61). A number of freshwater fish populations have been adversely
affected by nonnative species in many documented localities, several of
which were previously noted in the discussion under Factor A.
Bullfrogs were purposefully introduced nationwide in a concerted
effort to establish the species in all lakes and canal systems
throughout Mexico as a potential food source for humans although frog
legs ultimately never gained popularity in Mexican culinary culture
(Conant 1974, pp. 487-489). Rosen and Melendez (2006, p. 54) report
bullfrog invasions to be prevalent in northwestern Chihuahua and
northeastern Sonora where the northern Mexican gartersnake is thought
to occur. In many areas, native leopard frogs were completely displaced
(extirpated) where bullfrogs were observed. Rosen and Melendez (2006,
p. 54) also demonstrated the relationship between fish and amphibian
communities in Sonora and western Chihuahua in that 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
addition to bullfrog invasions, the first record in Mexico for the
nonnative Rio Grande leopard frog was recently documented in
northwestern Sonora, Mexico where the northern Mexican gartersnake is
considered likely extirpated (Rorabaugh and Servoss 2006, p. 102).
Unmack and Fagan (2004, p. 233) compared historical museum
collections of nonnative fish species from the Gila River basin in
Arizona and the geographically small Yaqui River basin
[[Page 56253]]
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
distribution, diversity, and abundance 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 and/or range reductions of native fish species are
expected to occur in the Yaqui Basin of Sonora, Mexico which may have
extant populations of northern Mexican gartersnake, as did much of the
Gila Basin before the introduction of nonnative species. The
implications of these declines in native fish to northern Mexican
gartersnakes indicate a potentially serious threat to the gartersnake's
persistence in these areas.
However, because specific and direct survey information is
significantly limited concerning the presence and potential effect of
nonnative species on the northern Mexican gartersnake in Mexico, this
discussion is based on extrapolation of how we understand these threats
to affect the subspecies in the United States. Furthermore, based on
the information available concerning the threats in Mexico we can not
conclude that the subspecies is likely to become endangered throughout
its range in Mexico. Although we acknowledge that these threats are
affecting the subpecies in the United States, we have determined that
the portion of the subspecies' range in the United States does not
constitute a significant portion of the range of the subspecies or a
DPS. Therefore, on the basis of the best available information, we
determine that it is not likely that the northern Mexican gartersnake
will become an endangered species within the foreseeable future based
on threats under this factor.
D. The Inadequacy of Existing Regulatory Mechanisms
Currently, the northern Mexican gartersnake is considered ``State
Endangered'' in New Mexico. In the State of New Mexico, an ``Endangered
Species'' is defined as ``any species of fish or wildlife whose
prospects of survival or recruitment within the state are in jeopardy
due to any of the following factors: (1) The present or threatened
destruction, modification or curtailment of its habitat; (2)
overutilization for scientific, commercial or sporting purposes; (3)
the effect of disease or predation; (4) other natural or man-made
factors affecting its prospects of survival or recruitment within the
state; or (5) any combination of the foregoing factors'' as per New
Mexico Statutory Authority (NMSA) 17-2-38.D. ``Take'', defined as
``means 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 northern Mexican gartersnakes, only
recommendations are afforded with respect to actions that result in
destruction or modification of habitat (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 gartersnakes per person per year as
specified in Commission Order Number 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 has subsequently amended Commission Order Number 43,
which closed the season on northern Mexican gartersnakes, effective
January 2005. Take of northern Mexican gartersnakes is no longer
permitted in Arizona without issuance of a scientific collecting permit
as per Arizona Administrative Code R12-4-401 et seq. While the Arizona
Game and Fish Department can seek criminal or civil penalties for
illegal take of northern Mexican gartersnakes, only recommendations are
afforded with respect to actions that result in destruction or
modification of northern Mexican gartersnake habitat.
As previously mentioned, humans encounter gartersnake species
somewhat regularly in riparian areas used for recreational purposes or
for other reasons. This is partially due to gartersnakes having an
active foraging strategy as well as diurnal behavior. Many such
encounters result in the capture, injury, or death of the gartersnake
due to the lay person's fear or dislike of 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). It would be very difficult for the
Arizona Game and Fish Department or the New Mexico Department of Fish
and Game to cite lay people (who are not reptile hobbyists or amateur
herpetologists in specific pursuit of herpetofauna) for such forms of
take. Consequently, while the pursuit and intentional collection of
reptiles, including the northern Mexican gartersnake, is regulated by
these agencies, unregulated capture, collection, or killing likely
occurs regularly.
We are reasonably certain that the level of illegal field
collecting by the hobbyist community is low because gartersnakes are
relatively undesirable in amateur herpetological collections. However,
there remains the possibility that small, isolated, and/or low-density
populations could be negatively affected by the collection of
reproductive females (Painter 2000, p. 39; Painter 2005; Holycross 2006).
The northern Mexican gartersnake is considered a ``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.
Neither the New Mexico Department of Game and Fish nor the Arizona
Game and Fish Department have specified or mandated recovery goals for
the northern Mexican gartersnake, nor has either State developed a
conservation agreement or plan for this species.
The U.S. Bureau of Land Management 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 the species
on Bureau of Land Management lands.
The presence of water is a primary habitat constituent for the
northern Mexican gartersnake. Public concern over the inadequacy of
Arizona surface water laws to ensure that flow is maintained perennial
streams was discussed by Arizona Republic columnist Shaun McKinnon
(2006b). McKinnon (2006b) highlighted the fact that because the
existing water laws are so old, they reflect a legislative
interpretation of the resource that is not consistent with what we know
today; yet the laws have never been updated or amended to account for
this discrepancy. For example, over 100
[[Page 56254]]
years ago when Arizona's water laws were written, the important
connection between groundwater and surface water was not known
(McKinnon 2006b). Furthermore, meaningful changes to these regulations
that account for the relative scarcity of surface water are unlikely to
come about because Arizona is so ``entrenched in tradition and in
property ownership'' and because the threat of litigation over proposed
changes precludes such efforts (McKinnon 2006b). McKinnon (2006b)
specifically, mentions the Gila, Salt, Verde, Santa Cruz, and San Pedro
rivers as having habitat attributes that have directly suffered from
inadequate surface water regulations.
The U.S. Forest Service does not include northern Mexican
gartersnake on their ``Management Indicator Species List,'' but it is
included on the ``Regional Forester's Sensitive Species List.'' This
means that northern Mexican gartersnakes are ``considered'' in land
management decisions. Individual U.S. Forest Service biologists may
opportunistically gather data on the gartersnakes observed incidentally
in the field for their records, although it is not required.
Activities that could adversely affect northern Mexican
gartersnakes and their habitat continue to occur throughout their
extant distribution on U.S. Forest Service lands. Clary and Webster
(1989, p. 1) stated that ``* * * most riparian grazing results suggest
that the specific grazing system used is not of dominant importance,
but good management is--with control of use in the riparian area a key
item.'' Due to ongoing constraints in funding, staff levels, and time,
and regulatory compliance pertaining to monitoring and reporting duties
tied to land management, proactive measures continue to be limited.
These factors affect a land manager's ability to employ adaptive
management procedures when effects to sensitive species or their
habitat could be occurring at levels greater than accounted for in
regulatory compliance mechanisms, such as in section 7 consultation
under the Act for other listed species that may co-occur with the
northern Mexican gartersnake in an area.
The majority of extant populations of northern Mexican gartersnake
in the United States occur on lands managed by the U.S. Bureau of Land
Management and U.S. Forest Service. Although both agencies have
riparian protection goals, neither agency has specific management plans
for the northern Mexican gartersnake.
Riparian communities are complex and recognized as unique in the
southwestern United States but are highly sensitive to many
anthropogenic land uses, as evidenced by the comparatively high number
of federally listed riparian or aquatic species. Four primary prey
species for the northern Mexican gartersnake, the Chiricahua leopard
frog, Gila topminnow, Gila chub, and roundtail chub, are federally
listed or were petitioned for listing. Other listed or proposed
riparian species or their proposed or designated critical habitat
overlap the current or historical distribution of the northern Mexican
gartersnake. Despite secondary protections that may be afforded to the
northern Mexican gartersnake from federally listed species and/or their
critical habitat, riparian and aquatic communities continue to be
adversely impacted for reasons previously discussed, contributing to
the declining status of the northern Mexican gartersnake throughout its
range in the United States.
Throughout Mexico, the Mexican gartersnake is federally 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 time frame, if the factors that impact negatively their
viability, cause the deterioration or modification of their habitat or
directly diminish directly 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 (42 U.S.C. 4321 et seq.). This Mexican regulation
requires an environmental assessment of private or government actions
that may affect wildlife and/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, 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
recently developed the Method of Evaluation of the Risk of Extinction
of the Wild Species in Mexico (MER) which unifies the criteria of
decision 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 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,
the Mexican gartersnake was placed on the NOM-059 [SEDESOL 1994 (NOM-
059-ECOL-1994), p. 46]
as a threatened species as determined by a panel
of scientific experts. However, we are uncertain of the specific
information that was used as the basis for the listing in Mexico and
were unable to obtain any information that was used to validate the
Federal listing of the Mexican gartersnake in Mexico.
Our review of the existing governmental regulatory mechanisms that
pertain to the management of the northern Mexican gartersnake or its
habitat in the United States leads us to conclude that the protections
afforded by existing regulations may be insufficient to adequately
address the declining status of the subspecies in the United States.
However, the Mexican gartersnake (inclusive of the northern Mexican
gartersnake) is considered a Federally-threatened species in Mexico.
Although we do not have sufficient information to analyze the efficacy
of existing regulatory mechanisms in Mexico, the best available data
does not support the conclusion that the species is likely to become in
danger of extinction within the foreseeable future due to the threats
posed by the other factors. Therefore, uncertainty with respect to the
efficacy of existing regulatory mechanisms is not dispositive as to the
listing status of the subspecies, and it is not a threatened species on
the basis of the lack of existing regulatory mechanisms.
[[Page 56255]]
E. Other Natural or Manmade Factors Affecting Its Continued Existence
in the United States
Marcy's checkered gartersnake (Thamnophis marcianus marcianus) may
have ecological implications in the decline and future conservation of
the northern Mexican gartersnake in southern Arizona. Marcy's checkered
gartersnake is a semi-terrestrial species that is able to co-exist to
some degree with riparian and aquatic nonnative predators. This is
largely due to its ability to forage in more terrestrial habitats,
specifically in the 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 bullfrogs,
nonnative sportfish, and crayfish also occur, which increases not only
the encounter rate between the species but also the juvenile mortality
rate of the northern Mexican gartersnake. Marcy's checkered gartersnake
is a potential benefactor of this scenario. As northern Mexican
gartersnake numbers decline within a population, space becomes
available for occupation by checkered gartersnakes. Marcy's checkered
gartersnake subsequently maintains pressure on the carrying capacity
(the maximum number of a given species that an area can maintain based
upon available resources) for an area and could potentially accelerate
the decline of 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 out-competing and replacing northern Mexican
gartersnakes at the San Bernardino National Refuge and surrounding
habitats of the Black Draw. They suspected that the drought 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 the decline of
the northern Mexican gartersnake. The ecological relationship between
these two species, in combination with other factors described above
that have adversely affected the northern Mexican gartersnake prey base
and the suitability of occupied and formerly occupied habitat, may be
contributing to the decline of this species.
We were unable to obtain any information on other natural or
manmade factors affecting the continued existence of the northern
Mexican gartersnake in Mexico.
Finding
We have carefully examined the best scientific and commercial
information available regarding the past, present, and future threats
faced by the northern Mexican gartersnake. We reviewed the petition,
information available in our files, other published and unpublished
information submitted to us during the public comment period following
our 90-day petition finding and consulted with recognized northern
Mexican gartersnake experts and other Federal, State, and Mexican
resource agencies. Because specific and direct survey information is
significantly limited concerning the presence and potential effect of
the threats discussed in this finding to the subspecies in Mexico, much
of our discussion is based on extrapolation of how we understand these
threats to affect the subspecies in the United States. Furthermore,
based on the information available concerning the threats in Mexico we
can not conclude that the subspecies is likely to become endangered
throughout its range in Mexico. Although we acknowledge that several
threats are affecting the subpecies in the United States, we have
determined that the portion of the subspecies' range in the United
States does not constitute a significant portion of the range of the
subspecies or a DPS. On the basis of the best scientific and commercial
information available, we determine that it is not likely that the
northern Mexican gartersnake is likely to become an endangered species
within the foreseeable future and that listing of the northern Mexican
gartersnake throughout its range in the United States and Mexico based
on its rangewide status is not warranted.
In making this finding, we respectfully acknowledge that the
Mexican government has found Thamnophis eques to be in danger of
disappearance in the short-or medium-term future in their country from
the destruction and modification of its habitat and/or from the effects
of shrinking population sizes and has therefore listed the species as
Threatened, under the listing authority of SEMARNAT (SEDESOL 2001).
However, as discussed at length in Factor D above, we also note that
the level of information required to list a species in Mexico may not
be as rigorous as that required to list a species in the United States
under the Endangered Species Act. Our conclusion that listing is not
warranted under the Act is based on: (1) The apparent differences in
listing protocols; (2) the significantly limited amount of information
available on the status of and threats to the northern Mexican
gartersnake in Mexico in comparison to our knowledge of the same in the
United States; and most importantly (3) the relatively large percentage
(70 to 80 percent) of the subspecies' historic distribution in Mexico
for which we have little to no information about with respect to status
and threats.
In making this Finding, we also recognize there have been declines
in the distribution and abundance of the northern Mexican gartersnake
within its distribution in the United States which are primarily
attributed to individual and community interactions with nonnative
species that occur in every locality where northern Mexican
gartersnakes have been documented in the United States. As discussed in
Factor C above, the documented mechanisms for which nonnative
interactions occur include: (1) Direct predation on northern Mexican
gartersnakes by nonnative species; and (2) the effects of a diminished
prey base via nonnative species preying upon and competing with native
prey species (Meffe 1985, pp. 179-185; Rosen and Schwalbe 1988, pp. 28-
31; 1995, p. 452; 2002b, pp. 223-227; Bestgen and Propst 1989, pp. 409-
410; Clarkson and Rorabaugh 1989, pp. 531, 535; Marsh and Minckley
1990, p. 265; Stefferud and Stefferud 1994, p. 364; Rosen et al. 1995,
pp. 257-258; 1996, pp. 2, 11-12; 2001, pp. 2, 21-22; Degenhardt et al.
1996, p. 319; Fernandez and Rosen 1996, pp. 21-33; Weedman and Young
1997, pp. 1, Appendices B, C; Inman et al. 1998, p. 17; Rinne et al.
1998, pp. 4-6; Fagan et al. 2005, pp. 38-39; Olden and Poff 2005, pp.
82-87; Holycross et al.2006, pp. 12-15; Brennan and Holycross 2006, p.
123). However, we again note that the portion of the historic
distribution of the northern Mexican gartersnake in the United States
represents approximately 20 to 30 percent of its rangewide
distribution. Furthermore, we were unable to obtain substantial
information regarding the status of the northern Mexican gartersnake in
Mexico (representing approximately 70 to 80 percent of its rangewide
distribution).
Throughout the range of the northern Mexican gartersnake, but most
accurately within its distribution in the United States, literature
documents the cause and effect relationship of disturbances to the
trophic structure (food chain) of native riparian and aquatic
communities. The substantial decline of primary native prey species,
such as leopard frogs and native fish, has contributed significantly to
the decline of a primary predator, the northern Mexican gartersnake. In
this
[[Page 56256]]
respect, the northern Mexican gartersnake is considered an indicator
species, or a species that can be used to gauge the condition of a
particular habitat, community, or ecosystem. The synergistic effect of
nonnative species both reducing the prey base of, and directly preying
upon, northern Mexican gartersnakes has placed significant pressure
upon the viability and sustainability of extant northern Mexican
gartersnake populations and has led to significant fragmentation and
risks to the continued viability of extant populations. The
evolutionary biology of the northern Mexican gartersnake, much like
that of native fish and leopard frogs, has left the species without
adaptation to and defenseless against the effect of nonnative species
invasions.
We further recognize that in addition to the deleterious effects of
nonnative species invasions, the decline of the northern Mexican
gartersnake has been exacerbated by historical and ongoing threats to
its habitat in the United States. The threats identified and discussed
above in detail in Factor A, ``The Present or Threatened Destruction,
Modification, or Curtailment of its Habitat or Range,'' effectively
summarize our knowledge of the current and future status of its
riparian and aquatic habitat in the United States. Chiefly, these
threats include: (1) The modification and loss of ecologically valuable
cienegas (Hendrickson and Minckley 1984, p. 161; Stromberg et al. 1996,
p. 113); (2) urban and rural development (Medina 1990, p. 351;
Girmendock and Young 1997, pp. 45-47; Voeltz 2002, p. 88; Wheeler et
al. 2005, pp. 153-154); (3) road construction, use, and maintenance
(Rosen and Lowe 1994, pp. 143, 146-148; Waters 1995, p. 42; Carr and
Fahrig 2001, pp. 1074-1076; Hels and Buchwald 2001, p. 331; Smith and
Dodd 2003, pp. 134-138; Angermeier et al. 2004, p. 19; Shine et al.
2004, pp. 9, 17-19; Andrews and Gibbons 2005, p. 772; Wheeler et al.
2005, pp. 145, 148-149; Roe et al. 2006, pp. 163-166); (4) human
population growth (Girmendock and Young 1993, p. 47; American Rivers
2006; Arizona Republic, March 16, 2006); (5) groundwater pumping,
surface water diversions, and drought (Abarca and Weedman 1993, p. 2;
Girmendock and Young 1993, pp. 45-52; Sullivan and Richardson 1993, pp.
35-42; Stromberg et al. 1996, pp. 124-127; Boulton et al. 1998, pp. 60-
62; Rinne et al. 1998, pp. 7-11; Voeltz 2002, p. 88; Philips and Thomas
2005; Webb and Leake 2005, pp. 307-308; American Rivers 2006; Boulton
and Hancock 2006, p. 139); (6) improper livestock grazing (Sartz and
Tolsted 1974, p. 354; Kauffman and Krueger 1984, pp. 433-434; Szaro et
al. 1985, pp. 361-363; Weltz and Wood 1986, p. 367-368; Clary and
Webster 1989, pp. 1-3; Clary and Medin 1990, pp. 1-6; Orodho et al.
1990, p. 9; Fleischner 1994; pp. 631-632; Trimble and Mendel 1995, p.
233; Waters 1995, pp. 22-24; Girmendock and Young 1997, p. 47; Pearce
et al. 1998, p. 302; Belsky et al. 1999, p. 1; Voeltz 2002, p. 88;
Krueper et al. 2003, pp. 607, 613-614); (7) catastrophic wildfire and
wildfire in non-fire adapted communities (Rinne and Neary 1996, p. 135;
Esque and Schwalbe 2002, pp. 165, 190); and (8) undocumented
immigration and international border enforcement and management
activities (Segee and Neeley 2006, pp. 5-7; USFWS 2006, pp. 91-105).
In our discussion under Factors A through E above, we have provided
a comprehensive, in-depth analysis of all known threats that have or
continue to affect the status of the northern Mexican gartersnake in
the United States, including those which have not yet been documented
but where potential effects exist. As a result of our assessment, we
note that certain land use activities such as road construction and
use, direct mortality from livestock grazing, undocumented immigration
and international border enforcement and management activities, and
some types of development, pose a more significant risk to highly
fragmented, low density populations of northern Mexican gartersnakes.
As noted on several occasions above, in these types of situations where
the viability of a known northern Mexican gartersnake population is
clearly at risk, the loss of a single reproductive female due to these
threats is of concern. However, these types of threats are less
significant to the northern Mexican gartersnake when the status of
these at-risk populations improves through the implementation of
conservation activities. We also remain optimistic that our local,
State, and Federal partners in wildlife conservation will be proactive
in monitoring populations and implementing conservation measures to
ensure that apparent declines of the northern Mexican gartersnake in
the United States are reversed and that this species remains a member
of our native riparian and aquatic communities. But we do not rely upon
any future conservation actions in making this finding.
Notwithstanding our extensive discussion of the past and ongoing
threats affecting this species, and the evidence of range contraction
within the United States, neither the existence of the threats nor past
range contraction means that a species meets the definition of a
threatened or endangered species under the Act. Based on our evaluation
of the best available data, we conclude that the northern Mexican
gartersnake is not likely to become an endangered species in all or a
significant portion of its range in the foreseeable future.
References Cited
A complete list of all references cited in this document is
available upon request from the Field Supervisor at the Arizona
Ecological Services Office (see ADDRESSES section).
Author
The primary author of this document is the Arizona Ecological
Services Office (see ADDRESSES section).
Authority: The authority for this action is the Endangered
Species Act of 1973, as amended (16 U.S.C. 1531 et seq.).
Dated: September 14, 2006.
H. Dale Hall,
Director, Fish and Wildlife Service.
[FR Doc. 06-7784 Filed 9-25-06; 8:45 am]
BILLING CODE 4310-55-P