Endangered and Threatened Wildlife and Plants; Threatened Status for the Northern Mexican Gartersnake and Narrow-headed Gartersnake

DEPARTMENT OF THE INTERIOR

Fish and Wildlife Service

50 CFR Part 17

[Docket No. FWS-R2-ES-2013-0071; 4500030113]

RIN 1018-AY23

Endangered and Threatened Wildlife and Plants; Threatened Status for the Northern Mexican Gartersnake and Narrow-headed Gartersnake

AGENCY:

Fish and Wildlife Service, Interior.

ACTION:

Proposed rule.

SUMMARY:

We, the U.S. Fish and Wildlife Service (Service), propose to list the northern Mexican gartersnake (

Thamnophis eques megalops

) and narrow-headed gartersnake (

Thamnophis rufipunctatus

) as threatened species under the Endangered Species Act of 1973, as amended (Act). If we finalize this rule as proposed, it would extend the Act's protections to these species. The effect of this regulation is to conserve northern Mexican and narrow-headed gartersnakes under the Act.

DATES:

We will accept comments received or postmarked on or before September 9, 2013. Comments submitted electronically using the Federal eRulemaking Portal (see

ADDRESSES

section, below) must be received by 11:59 p.m. Eastern Time on the closing date. We must receive requests for public hearings, in writing, at the address shown in the

FOR FURTHER INFORMATION CONTACT

section by August 26, 2013.

ADDRESSES:

You may submit comments by one of the following methods:

(1)

Electronically:

Go to the Federal eRulemaking Portal:

http://www.regulations.gov.

Search for Docket No. FWS-R2-ES-2013-0071, which is the docket number for this rulemaking. When you locate this document, you may submit a comment by clicking on “Comment Now!”

(2)

By hard copy:

Submit by U.S. mail or hand-delivery to: Public Comments Processing, Attn: FWS-R2-ES-2013-0071; Division of Policy and Directives Management; U.S. Fish and Wildlife Service; 4401 N. Fairfax Drive, MS 2042-PDM; Arlington, VA 22203.

We request that you send comments only by the methods described above. We will post all comments on

http://www.regulations.gov.

This generally means that we will post any personal information you provide us (see the Information Requested section below for more information).

FOR FURTHER INFORMATION CONTACT:

Steve Spangle, Field Supervisor, U.S. Fish and Wildlife Service, Arizona Ecological Services Field Office, 2321 West Royal Palm Road, Suite 103, Phoenix, AZ 85021; telephone: 602-242-0210; facsimile: 602-242-2513. If you use a telecommunications device for the deaf (TDD), call the Federal Information Relay Service (FIRS) at 800-877-8339.

SUPPLEMENTARY INFORMATION:

Executive Summary

Why we need to publish a rule.

Under the Endangered Species Act (Act), if a species is determined to be an endangered or threatened species throughout all or a significant portion of its range, we are required to promptly publish a proposal in the

Federal Register

and make a determination on our proposal within one year. Listing a species as an endangered or threatened species can only be completed by issuing a rule. Elsewhere in today's

Federal Register

, we propose to designate critical habitat for the northern Mexican and narrow-headed gartersnakes under the Act.

This document consists of:

• A proposed rule to list the northern Mexican and narrow-headed gartersnakes as threatened species throughout their ranges, and

• A proposed special rule under section 4(d) under the Act that outlines the prohibitions necessary and advisable for the conservation of the northern Mexican gartersnake.

The basis for our action.

Under the Act, we can determine that a species is an endangered or threatened species based on any of five factors: (A) The present or threatened destruction, modification, or curtailment of its habitat or range; (B) overutilization for commercial, recreational, scientific, or educational purposes; (C) disease or predation; (D) the inadequacy of existing regulatory mechanisms; or (E) other natural or manmade factors affecting its continued existence. In the case of the northern Mexican and narrow-headed gartersnakes, we have determined that harmful nonnative species (spiny-rayed fish, bullfrogs, and crayfish), wildfires, and land uses that divert, dry up, or significantly pollute aquatic habitat have solely or collectively affected these gartersnakes, and several of their native prey species, such that their resiliency, redundancy, and representation across their ranges have been significantly compromised.

We will seek peer review.

We are seeking comments from knowledgeable individuals with scientific expertise to review our analysis of the best available science and application of that science and to provide any additional scientific information to improve this proposed rule. Because we will consider all comments and information received during the comment period, our final determinations may differ from this proposal.

Information Requested

We intend that any final action resulting from this proposed rule will be based on the best scientific and commercial data available and be as accurate and as effective as possible. Therefore, we request comments or information from other concerned governmental agencies, Native American tribes, the scientific community, industry, or any other interested parties concerning this proposed rule. We particularly seek comments concerning:

(1) The species' biology, range, and population trends, including:

(a) Habitat requirements for feeding, breeding, and sheltering;

(b) Genetics and taxonomy;

(c) Historical and current range, including distribution patterns;

(d) Historical and current population levels, and current and projected trends; and

(e) Past and ongoing conservation measures for these species, their habitat or both.

(2) The factors that are the basis for making a listing determination for these species under section 4(a) of the Act (16 U.S.C. 1531

et seq.

), which are:

(a) The present or threatened destruction, modification, or curtailment of its habitat or range;

(b) Overutilization for commercial, recreational, scientific, or educational purposes;

(c) Disease or predation;

(d) The inadequacy of existing regulatory mechanisms; or

(e) Other natural or manmade factors affecting its continued existence.

(3) Biological, commercial trade, or other relevant data concerning any threats (or lack thereof) to these species and existing regulations that may be addressing those threats.

(4) Additional information concerning the historical and current status, range, distribution, and population size of these species, including the locations of any additional populations of these species.

(5) Any information on the biological or ecological requirements of these species, and ongoing conservation measures for the species and their habitats.

(6) Any information on the projected and reasonably likely impacts of climate

change on the northern Mexican gartersnake and narrow-headed gartersnake.

Please include sufficient information with your submission (such as scientific journal articles or other publications) to allow us to verify any scientific or commercial information you include.

Please note that submissions merely stating support for or opposition to the action under consideration without providing supporting information, although noted, will not be considered in making a determination, as section 4(b)(1)(A) of the Act directs that determinations as to whether any species is a threatened or endangered species must be made “solely on the basis of the best scientific and commercial data available.”

You may submit your comments and materials concerning this proposed rule by one of the methods listed in the

ADDRESSES

section. We request that you send comments only by the methods described in the

ADDRESSES

section.

If you submit information via

http://www.regulations.gov,

your entire submission—including any personal identifying information—will be posted on the Web site. If your submission is made via a hardcopy that includes personal identifying information, you may request at the top of your document that we withhold this information from public review. However, we cannot guarantee that we will be able to do so. We will post all hardcopy submissions on

http://www.regulations.gov.

Please include sufficient information with your comments to allow us to verify any scientific or commercial information you include.

Comments and materials we receive, as well as supporting documentation we used in preparing this proposed rule, will be available for public inspection on

http://www.regulations.gov,

or by appointment, during normal business hours, at the U.S. Fish and Wildlife Service, Arizona Ecological Services Field Office (see

FOR FURTHER INFORMATION CONTACT

).

Previous Federal Actions

The northern Mexican and narrow-headed gartersnakes were placed on the list of candidate species as Category 2 species on September 18, 1985 (50 FR 37958). Category 2 species were those for which existing information indicated that listing was possibly appropriate, but for which substantial supporting biological data to prepare a proposed rule were lacking. In the 1996 Candidate Notice of Review (February 28, 1996; 61 FR 7596), the use of Category 2 candidates was discontinued, and the northern Mexican and narrow-headed gartersnakes were no longer recognized as candidates.

On December 19, 2003, we received a petition from the Center for Biological Diversity (“petitioner”) dated December 15, 2003, requesting that we list the northern Mexican gartersnake as threatened or endangered, and that we designate critical habitat concurrently with the listing. The petition was clearly identified as a petition for a listing rule and contained the names, signatures, and addresses of the requesting parties. Included in the petition was supporting information regarding the species' taxonomy and ecology, historical and current distribution, present status, and actual and potential causes of decline. We acknowledged the receipt of the petition in a letter to the petitioner, dated March 1, 2004. In that letter, we also advised that, due to funding constraints in fiscal year (FY) 2004, we would not be able to begin processing the petition at that time.

On May 17, 2005, the petitioner filed a complaint for declaratory and injunctive relief, challenging our failure to issue a 90-day finding for the northern Mexican gartersnake in response to the petition as required by 16 U.S.C. 1533(b)(3)(A) and (B). In a stipulated settlement agreement, we agreed to submit a 90-day finding to the

Federal Register

by December 16, 2005, and if substantial, submit a 12-month finding to the

Federal Register

by September 15, 2006 (

Center for Biological Diversity

v.

Norton,

CV-05-341-TUC-CKJ (D. Az)). The settlement agreement was signed and adopted by the District Court of Arizona on August 2, 2005.

On December 13, 2005, we made our 90-day finding that the petition presented substantial scientific information indicating that listing the northern Mexican gartersnake may be warranted; the finding and our initiation of a status review was published in the

Federal Register

on January 4, 2006 (71 FR 315).

On September 26, 2006, we published a 12-month finding that listing of the northern Mexican gartersnake was not warranted because we determined that not enough information on the subspecies' status and threats in Mexico was known at that time (71 FR 56227). On November 17, 2007, the petitioner filed a complaint for declaratory and injunctive relief pursuant to section 11 of the Act (16 U.S.C. 1540), seeking to set aside the 12-month finding. Additionally, a formal opinion was issued by the Solicitor of the Department of the Interior, “The Meaning of In Danger of Extinction Throughout All or a Significant Portion of Its Range” (U.S. DOI 2007), which provides further guidance on how to conduct a detailed analysis of whether a species is in danger of extinction throughout a significant portion of its range. In December 2007, the Service withdrew the September 26, 2006, 12-month finding in order to consider the new “Significant Portion of the Range” policy. In a stipulated settlement agreement with the petitioner, we agreed to submit a new 12-month finding to the

Federal Register

by November 17, 2008 (

Center for Biological Diversity

v.

Kempthorne,

CV-07-596-TUC-RCCJ (D. Az)). The settlement agreement was signed and adopted by the District Court of Arizona on June 18, 2008.

On May 28, 2008, we published notice (73 FR 30596) of our intent to initiate a status review for the northern Mexican gartersnake and solicited the public for information on the status of, and potential threats to, this species.

On November 25, 2008, we published a second 12-month finding that listing of the northern Mexican gartersnake was warranted but precluded by other listing priorities at that time (73 FR 71788). The petitioner described three potentially listable entities of northern Mexican gartersnake for consideration by the Service: (1) Listing the U.S. population as a distinct population segment (DPS); (2) listing the subspecies throughout its range in the United States and Mexico based on its rangewide status; or (3) listing the subspecies throughout its range in the United States and Mexico based on its status in the United States. Because we found that listing the northern Mexican gartersnake rangewide was warranted, there was no need to conduct any further analysis of the remaining two options, which are smaller geographic entities and are subsumed by the rangewide listing.

Status Assessments for Northern Mexican and Narrow-headed Gartersnakes

Background

Northern Mexican Gartersnake

Subspecies Description

The northern Mexican gartersnake ranges in color from olive to olive-brown or olive-gray with three lighter-colored stripes that run the length of the body, the middle of which darkens towards the tail. It may occur with other native gartersnake species and can be difficult for people without specific expertise to identify. The snake may reach a maximum known length of 44 inches (in) (112 centimeters (cm)). The pale yellow to light-tan lateral (side of

body) stripes distinguish the northern Mexican gartersnake from other sympatric (co-occurring) gartersnake species because a portion of the lateral stripe is found on the fourth scale row, while it is confined to lower scale rows for other species. Paired black spots extend along the olive dorsolateral fields (region adjacent to the top of the snake's back) and the olive-gray ventrolateral fields (region adjacent to the area of the snake's body in contact with the ground). The scales are keeled (possessing a ridge down the center of each scale). A more detailed subspecies description can be found in our September 26, 2006 (71 FR 56227), or November 25, 2008 (73 FR 71788) 12-month findings for this subspecies, or by reviewing Rosen and Schwalbe (1988, p. 4), Rossman

et al.

(1996, pp. 171-172), Ernst and Ernst (2003, pp. 391-392), or Manjarrez and Garcia (1993, pp. 1-5).

Taxonomy

The northern Mexican gartersnake is a member of the family Colubridae and subfamily Natricinae (harmless live-bearing snakes) (Lawson

et al.

2005, p. 596). The taxonomy of the genus

Thamnophis

has a complex history, partly because many of the species are similar in appearance and arrangement of scales, but also because many of the early museum specimens were in such poor and faded condition that it was difficult to study them (Conant 2003, p. 6).

Prior to 2003,

Thamnophis eques

was considered to have three subspecies,

T. e. eques, T. e. megalops,

and

T. e. virgatenuis

(Rossman

et al.

1996, p. 175). In 2003, an additional seven new subspecies were identified under

T. eques

: (1)

T. e. cuitzeoensis

; (2)

T. e. patzcuaroensis

; (3)

T. e. insperatus

; (4)

T. e. obscurus

; (5)

T. e. diluvialis

; (6)

T. e. carmenensis

; and (7)

T. e. scotti

(Conant 2003, p. 3). Common names were not provided, so in this proposed rule, we use the scientific name for all subspecies of Mexican gartersnake other than the northern Mexican gartersnake. These seven new subspecies were described based on morphological differences in coloration and pattern; have highly restricted distributions; and occur in isolated wetland habitats within the mountainous Transvolcanic Belt region of southern Mexico, which contains the highest elevations in the country (Conant 2003, pp. 7-8). The validity of the current taxonomy of the 10 subspecies of

T. eques

is accepted within the scientific community. A more detailed description of the taxonomy of the northern Mexican gartersnake is found in our September 26, 2006 (71 FR 56227) and November 25, 2008 (73 FR 71788) 12-month findings for this subspecies. Additional information regarding this subspecies' taxonomy can be found in de Queiroz

et al.

(2002, p. 323), de Queiroz and Lawson (1994, p. 217), Rossman

et al.

(1996, pp. xvii-xviii, 171-175), Rosen and Schwalbe (1988, pp. 2-3), Liner (1994, p. 107), and Crother

et al.

(2012, p. 70).

Habitat and Natural History

Throughout its rangewide distribution, the northern Mexican gartersnake occurs at elevations from 130 to 8,497 feet (ft) (40 to 2,590 meters (m)) (Rossman

et al.

1996, p. 172) and is considered a “terrestrial-aquatic generalist” by Drummond and Marcías-García (1983, pp. 24-26). The northern Mexican gartersnake is a riparian obligate (restricted to riparian areas when not engaged in dispersal behavior) and occurs chiefly in the following general habitat types: (1) Source-area wetlands (e.g., cienegas (mid-elevation wetlands with highly organic, reducing (basic or alkaline) soils), or stock tanks (small earthen impoundment)); (2) large-river riparian woodlands and forests; and (3) streamside gallery forests (as defined by well-developed broadleaf deciduous riparian forests with limited, if any, herbaceous ground cover or dense grass) (Hendrickson and Minckley 1984, p. 131; Rosen and Schwalbe 1988, pp. 14-16). Emmons and Nowak (2013, p. 14) found this subspecies most commonly in protected backwaters, braided side channels and beaver ponds, isolated pools near the river mainstem, and edges of dense emergent vegetation that offered cover and foraging opportunities when surveying in the upper Verde River region. Additional information on the habitat requirements of the northern Mexican gartersnake within the United States and Mexico can be found in our 2006 (71 FR 56227) and 2008 (73 FR 71788) 12-month findings for this subspecies and in Rosen and Schwalbe (1988, pp. 14-16), Rossman

et al.

(1996, p. 176), McCranie and Wilson (1987, pp. 11-17), Ernst and Ernst (2003, p. 392), and Cirett-Galan (1996, p. 156).

The northern Mexican gartersnake is surface active at ambient (air) temperatures ranging from 71 degrees Fahrenheit (°F) to 91 °F (22 degrees Celsius (°C) to 33 °C) and forages along the banks of waterbodies (Rosen 1991, p. 305, Table 2). Rosen (1991, pp. 308-309) found that northern Mexican gartersnakes spent approximately 60 percent of their time moving, 13 percent of their time basking on vegetation, 18 percent of their time basking on the ground, and 9 percent of their time under surface cover; body temperatures ranged from 75 to 91 °F (24 to 33 °C) and averaged 82 °F (28 °C), which is lower than other, similar species with comparable habitat and prey preferences. Rosen (1991, p. 310) suggested that lower preferred body temperatures exhibited by northern Mexican gartersnakes may be due to: (1) Their tendency to occupy cienega-like habitat, where warm air temperatures are relatively unavailable; and (2) their tendency to remain in dense cover. In the northern-most part of its range, the northern Mexican gartersnake appears to be most active during July and August, followed by June and September.

The northern Mexican gartersnake is an active predator and is believed to heavily depend upon a native prey base (Rosen and Schwalbe 1988, pp. 18, 20). Northern Mexican gartersnakes forage along vegetated banklines, searching for prey in water and on land, using different strategies (Alfaro 2002, p. 209). Generally, its diet consists of amphibians and fishes, such as adult and larval (tadpoles) native leopard frogs (e.g., lowland leopard frog (

Lithobates yavapaiensis

) and Chiricahua leopard frog (

Lithobates chiricahuensis

)), as well as juvenile and adult native fish species (e.g., Gila topminnow (

Poeciliopsis occidentalis occidentalis

), desert pupfish (

Cyprinodon macularius

), Gila chub (

Gila intermedia

), and roundtail chub (

Gila robusta

)) (Rosen and Schwalbe 1988, p. 18). Drummond and Marcías-García (1983, pp. 25, 30) found that as a subspecies, Mexican gartersnakes fed primarily on frogs. Auxiliary prey items may also include young Woodhouse's toads (

Anaxyrus woodhousei

), treefrogs (Family Hylidae), earthworms, deermice (

Peromyscus

spp.), lizards of the genera

Aspidoscelis

and

Sceloporus,

larval tiger salamanders (

Ambystoma tigrinum

), and leeches (Gregory

et al.

1980, pp. 87, 90-92; Rosen and Schwalbe 1988, p. 20; Holm and Lowe 1995, pp. 30-31; Degenhardt

et al.

1996, p. 318; Rossman

et al.

1996, p. 176; Manjarrez 1998, p. 465). In situations where native prey species are rare or absent, this snake's diet may include nonnative species, including larval and juvenile bullfrogs (

Lithobates catesbeianus

), mosquitofish (

Gambusia affinis

) (Holycross

et al.

2006, p. 23; Emmons and Nowak 2013, p. 5), or other soft-rayed fish species. Chinese mystery snails (

Cipangopaludina chinensis

) have been reported as a prey item for northern Mexican gartersnakes at the Page Springs and Bubbling Ponds State Fish

Hatcheries in Arizona, but some predation attempts on snails have proven fatal for gartersnakes because of their lower jaw becoming permanently lodged in the snails' shell (Young and Boyarski 2012, p. 498). Venegas-Barrera and Manjarrez (2001, p. 187) reported the first observation of a snake in the natural diet of any species of

Thamnophis

after documenting the consumption by a Mexican gartersnake (subspecies not provided) of a Mexican alpine blotched gartersnake (

Thamnophis scalaris

).

Marcías-García and Drummond (1988, pp. 129-134) sampled the stomach contents of Mexican gartersnakes and the prey populations at (ephemeral) Lake Tecocomulco, Hidalgo, Mexico. Field observations indicated, with high statistical significance, that larger Mexican gartersnakes fed primarily upon aquatic vertebrates (fishes, frogs, and larval salamanders) and leeches, whereas smaller Mexican gartersnakes fed primarily upon earthworms and leeches (Marcías-García and Drummond 1988, p. 131). Marcías-García and Drummond (1988, p. 130) also found that the birth of newborn

T. eques

tended to coincide with the annual peak density of annelids (earthworms and leeches). There is also preliminary evidence that birth may coincide with a pronounced influx of available prey in a given area, especially with that of explosive breeders, such as toads, but more research is needed to confirm such a relationship (Boyarski 2012, pers. comm.). Positive correlations were also made with respect to capture rates (which are correlated with population size) of

T. eques

to lake levels and to prey scarcity; that is, when lake levels were low and prey species scarce, Mexican gartersnake capture rates declined (Marcías-García and Drummond 1988, p. 132). This indicates the importance of available water and an adequate prey base to maintaining viable populations of Mexican gartersnakes. Marcías-García and Drummond (1988, p. 133) found that while certain prey items were positively associated with size classes of snakes, the largest of specimens consume any prey available.

Native predators of the northern Mexican gartersnake include birds of prey, other snakes (kingsnakes (

Lampropeltis

sp.), whipsnakes (

Coluber

sp.), regal ring-necked snakes (

Diadophis punctatus regalis

), etc.), wading birds, mergansers (

Mergus merganser

), belted kingfishers (

Megaceryle alcyon

), raccoons (

Procyon lotor

), skunks (

Mephitis

sp.), and coyotes (

Canis latrans

) (Rosen and Schwalbe 1988, pp. 18, 39; Brennan

et al.

2009, p. 123). Historically, large, highly predatory native fish species such as Colorado pikeminnow may have preyed upon northern Mexican gartersnake where the subspecies co-occurred. Native chubs (

Gila

sp.) may also prey on neonatal gartersnakes.

Parasites have been observed in northern Mexican gartersnakes. Boyarski (2008b, pp. 5-6) recorded several snakes within the population at the Page Springs and Bubbling Ponds fish hatcheries with interior bumps or bulges along the anterior one-third of the body. The cause of these bumps was not identified or speculated upon, nor were there any signs of trauma to the body of these snakes in the affected areas. Dr. Jim Jarchow, a veterinarian with herpetological expertise, reviewed photographs of affected specimens and suggested the bumps may likely contain plerocercoid larvae of a pseudophyllidean tapeworm (possibly

Spirometra

spp.), which are common in fish- and frog-eating gartersnakes. This may not be detrimental to their health, provided the bumps do not grow large enough to impair movement or other bodily functions (Boyarski 2008b, p. 8). However, Gúzman (2008, p. 102) documented the first observation of mortality of a Mexican gartersnake from a larval

Eustrongylides

sp. (endoparasitic nematode) which “raises the possibility that infection of Mexican gartersnakes by

Eustrongylides

sp. larvae might cause mortality in some wild populations,” especially if those populations are under stress as a result of the presence of other threats.

Sexual maturity in northern Mexican gartersnakes occurs at 2 years of age in males and at 2 to 3 years of age in females (Rosen and Schwalbe 1988, pp. 16-17). Northern Mexican gartersnakes are viviparous (bringing forth living young rather than eggs). Mating has been documented in April and May followed by the live birth of between 7 and 38 newborns (average is 13.6) in July and August (Rosen and Schwalbe 1988, p. 16; Nowak and Boyarski 2012, pp. 351-352). However, field observations in Arizona provide preliminary evidence that mating may also occur during the fall, but further research is required to confirm this hypothesis (Boyarski 2012, pers. comm.). Unlike other gartersnake species, which typically breed annually, one study suggests that only half of the sexually mature females within a population of northern Mexican gartersnake might reproduce in any one season (Rosen and Schwalbe 1988, p. 17).

Historical Distribution

Within the United States, the northern Mexican gartersnake historically occurred predominantly in Arizona at elevations ranging from 130 to 6,150 ft (40 to 1,875 m). It was generally found where water was relatively permanent and supported suitable habitat. The northern Mexican gartersnake historically occurred in every county and nearly every subbasin within Arizona, from several perennial or intermittent creeks, streams, and rivers as well as lentic (still, non-flowing water) wetlands such as cienegas, ponds, or stock tanks. Northern Mexican gartersnake records exist within the following subbasins in Arizona: Colorado River, Bill Williams River, Agua Fria River, Salt River, Tonto Creek, Verde River, Santa Cruz River, Cienega Creek, San Pedro River, Babocomari River, and the Rio San Bernardino (Black Draw) (Woodin 1950, p. 40; Nickerson and Mays 1970, p. 503; Bradley 1986, p. 67; Rosen and Schwalbe 1988, Appendix I; 1995, p. 452; 1997, pp. 16-17; Holm and Lowe 1995, pp. 27-35; Sredl

et al.

1995b, p. 2; 2000, p. 9; Rosen

et al.

2001, Appendix I; Holycross

et al.

2006, pp. 1-2, 15-51; Brennan and Holycross 2006, p. 123; Radke 2006, pers. comm.; Rosen 2006, pers. comm.; Holycross 2006, pers. comm.; Cotton

et al.

2013, p. 111). Numerous records for the northern Mexican gartersnake (through 1996) in Arizona are maintained in the Arizona Game and Fish Department's (AGFD) Heritage Database (1996a).

Historically, the northern Mexican gartersnake had a limited distribution in New Mexico that consisted of scattered locations throughout the Upper Gila River watershed in Grant and western Hidalgo Counties, including the Upper Gila River, Mule Creek in the San Francisco River subbasin, and the Mimbres River (Price 1980, p. 39; Fitzgerald 1986, Table 2; Degenhardt

et al.

1996, p. 317; Holycross

et al.

2006, pp. 1-2).

One record for the northern Mexican gartersnake exists for the State of Nevada, opposite Fort Mohave, in Clark County along the shore of the Colorado River that was dated 1911 (De Queiroz and Smith 1996, p. 155). The subspecies may have occurred historically in the lower Colorado River region of California, although we were unable to verify any museum records for California. Any populations of northern Mexican gartersnakes that may have historically occurred in either Nevada or California were likely associated directly with the Colorado River, and

we believe them to be currently extirpated.

Within Mexico, northern Mexican gartersnakes historically occurred within the Sierra Madre Occidental and the Mexican Plateau in the Mexican states of Sonora, Chihuahua, Durango, Coahuila, Zacatecas, Guanajuato, Nayarit, Hidalgo, Jalisco, San Luis Potosí, Aguascalientes, Tlaxacala, Puebla, México, Veracruz, and Querétaro, comprising approximately 85 percent of the total rangewide distribution of the subspecies (Conant 1963, p. 473; 1974, pp. 469-470; Van Devender and Lowe 1977, p. 47; McCranie and Wilson 1987, p. 15; Rossman

et al.

1996, p. 173; Lemos-Espinal

et al.

2004, p. 83). We are not aware of any systematic, rangewide survey effort for the northern Mexican gartersnake in Mexico and have not found survey data for the subspecies in Mexico to be published in the scientific literature or otherwise readily available, outside of the information already obtained. Therefore, we use other, tightly correlated ecological surrogates (such as native freshwater fish) to inform discussion on the status of aquatic communities and aquatic habitat in Mexico, and therefore on the likely status of northern Mexican gartersnake populations. This discussion is found below in the subheadings pertinent to Mexico.

Current Distribution and Population Status

Where northern Mexican gartersnakes are locally abundant, they are usually reliably detected with significantly less effort than populations characterized as having low densities. Northern Mexican gartersnakes are well-camouflaged, secretive, and very difficult to detect in structurally complex, dense habitat where they could occur at very low population densities, which characterizes most occupied sites. Water clarity can also affect survey accuracy. We considered factors such as the date of the last known records for northern Mexican gartersnakes in an area, as well as records of one or more native prey species in making a conclusion on occupancy of the subspecies. We used the year 1980 to qualify occupancy because the 1980s marked the first systematic survey efforts for northern Mexican gartersnakes across their range (see Rosen and Schwalbe (1988, entire) and Fitzgerald (1986, entire)) and the last, previous records were often dated several decades prior and may not accurately represent the likelihood for current occupation. Several areas where northern Mexican gartersnakes were known to occur have received no, or very little, survey effort in the past several decades. Variability in survey design and effort makes it difficult to compare population sizes or trends among sites and between sampling periods. For each of the sites discussed in Appendix A (available at

http://www.regulations.gov

under Docket No. FWS-R2-ES-2013-0071), we have attempted to translate and quantify search and capture efforts into comparable units (

i.e.,

person-search hours and trap-hours) and have conservatively interpreted those results. Because the presence of suitable prey species in an area may provide evidence that the northern Mexican gartersnake may still persist in low density where survey data are sparse, a record of a native prey species was considered in our determination of occupancy of this subspecies.

Data on population status of northern Mexican gartersnakes in the United States are largely summarized in gray literature provided through agency reports and related documents. In our literature review efforts that resulted in our 2006 and 2008 12-month findings (71 FR 56227 and 73 FR 71788, respectively), we found that the status of the northern Mexican gartersnake has declined significantly in the last 30 years. We found that, in as much as 90 percent of the northern Mexican gartersnakes' historical distribution in the United States, the subspecies occurs at low to very low population densities or may even be extirpated. The decline of the northern Mexican gartersnake is primarily the result of predation by and competition with harmful nonnative species, such as spiny-rayed fish, bullfrogs, and crayfish, that have been intentionally released, accidentally released, or dispersed through natural mechanisms. Regardless of how they got into the wild, harmful nonnative species are now virtually ubiquitous throughout the range of the northern Mexican gartersnake. Land uses that result in the dewatering of habitat, combined with increasing drought, have destroyed significant amounts of habitat throughout the northern Mexican gartersnake's range and have also contributed to population declines.

Holycross

et al.

(2006, p. 66) detected the northern Mexican gartersnake at only 2 of 11 historical localities along the northern-most part of its range from which the subspecies was previously known. The only viable northern Mexican gartersnake populations in the United States where the subspecies remains reliably detected are all located in Arizona: (1) The Page Springs and Bubbling Ponds State Fish Hatcheries along Oak Creek, (2) lower Tonto Creek, (3) the upper Santa Cruz River in the San Rafael Valley, (4) the Bill Williams River, and (5) the upper Verde River. In New Mexico, the northern Mexican gartersnake may occur in extremely low population densities within its historical distribution; limited survey effort is inconclusive to determine extirpation. The status of the northern Mexican gartersnake on tribal lands, such as those owned by the White Mountain or San Carlos Apache Tribes, is poorly known due to historically limited survey access. As stated previously, less is known specifically about the current distribution of the northern Mexican gartersnake in Mexico due to limited access to information on survey efforts and field data from Mexico.

In Table 1 below, we summarize the population status of northern Mexican gartersnakes at all known localities throughout their United States distribution, as supported by museum records or reliable observations. For a detailed discussion that explains the rationale for site-by-site conclusions on occupancy, please see Appendix A (available at

http://www.regulations.gov

under Docket No. FWS-R2-ES-2013-0071). General rationale is provided in the introductory paragraph to this section, “Current Distribution and Population Status.”

Table 1—Current Population Status of the Northern Mexican Gartersnake in the United States. References Cited Are Provided in Appendix A

Location

Last record

Suitable physical habitat present

Native prey

species

present

Harmful nonnative species present

Population status

Gila River (NM, AZ)

2002

Yes

Yes

Yes

Likely not viable.

Spring Canyon (NM)

1937

Yes

Possible

Likely

Likely extirpated.

Mule Creek (NM)

1983

Yes

Yes

Yes

Likely not viable.

Mimbres River (NM)

Likely early 1900s

Yes

Yes

Yes

Likely extirpated.

Lower Colorado River (AZ)

1904

Yes

Yes

Yes

Likely extirpated.

Bill Williams River (AZ)

2012

Yes

Yes

Yes

Likely viable.

Agua Fria River (AZ)

1986

Yes

Yes

Yes

Likely not viable.

Little Ash Creek (AZ)

1984

Yes

Yes

Yes

Likely not viable.

Lower Salt River (AZ)

1964

Yes

Yes

Yes

Likely extirpated.

Black River (AZ)

1982

Yes

Yes

Yes

Likely not viable.

Big Bonito Creek (AZ)

1986

Yes

Yes

Yes

Likely not viable.

Tonto Creek (AZ)

2005

Yes

Yes

Yes

Likely viable.

Upper Verde River (AZ)

2012

Yes

Yes

Yes

Likely viable.

Oak Creek (AZ) (Page Springs and Bubbling Ponds State Fish Hatcheries)

2012

Yes

Yes

Yes

Likely viable.

Spring Creek (AZ)

1986

Yes

Yes

Yes

Likely not viable.

Sycamore Creek (AZ)

1954

Yes

Possible

Yes

Likely extirpated.

Upper Santa Cruz River/San Rafael Valley (AZ)

2012

Yes

Yes

Yes

Likely viable.

Redrock Canyon (AZ)

2008

Yes

Yes

Yes

Likely not viable.

Sonoita Creek (AZ)

1974

Yes

Possible

Yes

Likely extirpated.

Scotia Canyon (AZ)

2009

Yes

Yes

No

Likely not viable.

Parker Canyon (AZ)

1986

Yes

Possible

Yes

Likely not viable.

Las Cienegas National Conservation Area and Cienega Creek Natural Preserve (AZ)

2012

Yes

Yes

Possible

Likely not viable.

Lower Santa Cruz River (AZ)

1956

Yes

Yes

Yes

Likely extirpated.

Buenos Aires National Wildlife Refuge (AZ)

2000

Yes

Yes

Yes

Likely not viable.

Bear Creek (AZ)

1987

Yes

Yes

Yes

Likely not viable.

San Pedro River (AZ)

1996

Yes

Yes

Yes

Likely not viable.

Babocomari River and Cienega (AZ)

1986

Yes

Possible

Yes

Likely not viable.

Canelo Hills-Sonoita Grasslands Area (AZ)

2012

Yes

Yes

Yes

Likely not viable.

San Bernardino National Wildlife Refuge (AZ)

1997

Yes

Yes

Yes

Likely not viable.

Notes:

“Possible” means there were no conclusive data found. “Likely extirpated” means the last record for an area pre-dated 1980 and existing threats suggest the species is likely extirpated. “Likely not viable” means the last record for an area pre-dated 1980 and existing threats suggest the species is likely extirpated. “Likely viable” means that the species is reliably found with minimal to moderate survey effort and the population is generally considered viable.

Table 1 lists the 29 known localities for the northern Mexican gartersnake in the United States. Appendix A (available at

http://www.regulations.gov

under Docket No. FWS-R2-ES-2013-0071) discusses such considerations as the physical condition of habitat, the composition of the aquatic biological community, the existence of significant threats, and the length of time since the last known observation of the subspecies in presenting rationale for determining occupancy status at each locality. We have concluded that in as many as 24 of 29 known localities in the United States (83 percent), the northern Mexican gartersnake population is likely not viable and may exist at low population densities that could be threatened with extirpation or may already be extirpated. In most localities where the species may occur at low population densities, existing survey data are insufficient to prove extirpation. Only five populations of northern Mexican gartersnakes in the United States are considered likely viable where the species remains reliably detected. When considering the total number of stream miles in the United States that historically supported the northern Mexican gartersnake that are now permanently dewatered (except in the case of temporary flows in response to heavy precipitation), we concluded that as much as 90 percent of historical populations in the United States either occur at low densities or are extirpated. As displayed in Table 1, harmful nonnative species are a concern in almost every northern Mexican gartersnake locality in the United States and the most significant reason for their decline, as discussed in depth in our threats analysis below.

Listed as threatened throughout its range in Mexico by the Mexican Government, our understanding of the northern Mexican gartersnake's specific population status throughout its range in Mexico is less precise than that known for its United States distribution because survey efforts are less, and sufficient, available records do not exist or are difficult to obtain. However, we have assembled and reviewed an extensive body of scientific information on known, regional threats to northern Mexican gartersnakes and to their primary prey species. This information is presented in greater detail below in our specific discussion of threats to the species in Mexico.

Narrow-Headed Gartersnake

Species Description

The narrow-headed gartersnake is a small to medium-sized gartersnake with a maximum total length of 44 in (112 cm mm) (Painter and Hibbitts 1996, p. 147). Its eyes are set high on its unusually elongated head, which narrows to the snout, and it lacks striping on the dorsum (top) and sides, which distinguishes its appearance from other gartersnake species with which it could co-occur (Rosen and Schwalbe 1988, p. 7). The base color is usually tan or grey-brown (but may darken) with conspicuous brown, black, or reddish spots that become indistinct towards the

tail (Rosen and Schwalbe 1988, p. 7; Boundy 1994, p. 126). The scales are keeled. Degenhardt

et al.

(1996, p. 327), Rossman

et al.

(1996, pp. 242-244), and Ernst and Ernst (2003, p. 416) further describe the species.

Taxonomy

The narrow-headed gartersnake is a member of the family Colubridae and subfamily Natricinae (harmless live-bearing snakes) (Lawson

et al.

2005, p. 596). The taxonomy of the genus

Thamnophis

has a complex history partly because many of the species are similar in appearance and scutelation (arrangement of scales), but also because many of the early museum specimens were in such poor and faded condition that it was difficult to study them (Conant 2003, p. 6). The narrow-headed gartersnake has a particularly complex taxonomic history due to its morphology and feeding habits. There are approximately 30 species described in the gartersnake genus

Thamnophis

(Rossman

et al.

1996, pp. xvii-xviii). Two large overlapping clades (related taxonomic groups) of gartersnakes have been identified called the “Mexican” and “widespread” clades, supported by allozyme and mitochondrial DNA genetic analyses (de Queiroz

et al.

2002, p. 321).

Thamnophis rufipunctatus

is a member of the “Mexican” clade and is most closely related taxonomically to the southern Durango spotted gartersnake (

Thamnophis nigronuchalis

) (de Queiroz and Lawson 1994, p. 217; de Queiroz

et al.

2002; p. 321).

Due to the narrow-headed gartersnake's morphology and feeding habits, there has been considerable deliberation among taxonomists about the correct association of this species within seven various genera over time (Rosen and Schwalbe 1988, pp. 5-6); chiefly, between the genera

Thamnophis

(the “gartersnakes”) and

Nerodia

(the “watersnakes”) (Pierce 2007, p. 5). Chaisson and Lowe (1989, pp. 110-118) argued that the pattern of ultrastructural (as revealed by an electron microscope) pores in the scales of narrow-headed gartersnakes provided evidence that the species is more appropriately placed within the genus

Nerodia.

However, De Queiroz and Lawson (1994, p. 217) rejected this premise using mitochondrial DNA (mtDNA) genetic analyses to refute the inclusion of the narrow-headed gartersnake in the genus

Nerodia

and maintain the species within the genus

Thamnophis.

The narrow-headed gartersnake was first described as

Chilopoma rufipunctatum

by E. D. Cope (in Yarrow, 1875). Recently,

Thamnophis rufipunctatus nigronuchalis

and

T. r. unilabialis

were recognized as subspecies under

T. rufipunctatus

and comprised what was considered the

T. rufipunctatus

complex. However, Rossman

et al.

(1996, pp. 244-246) elevated

T. r. nigronuchalis

to full species designation and argued recognition of

T. r. unilabialis

be discontinued due to the diagnostic differences being too difficult to discern. Wood

et al.

(2011, p. 14) used genetic analysis of the

T. rufipunctatus

complex to propose the elevation of these three formerly recognized subspecies as three distinct species, as a result of a combination of interglacial warming, ecological and life-history constraints, and genetic drift, which promoted differentiation of these three species throughout the warming and cooling periods of the Pleistocene epoch (Wood

et al.

2011, p. 15). We use these most recent and complete data in acknowledging these three entities as unique species:

T. rufipunctatus

(along the Mogollon Rim of Arizona and New Mexico),

T. unilabialis

(Chihuahua, eastern Sonora, and northern Durango, Mexico), and

T. nigronuchalis

(southern Durango, Mexico).

Several common names have been used for this species including the red-spotted gartersnake, the brown-spotted gartersnake, and the currently used, narrow-headed gartersnake (Rosen and Schwalbe 1988, p. 5). Further discussion of the taxonomic history of the narrow-headed gartersnake is available in Crother (2012, p. 71), Degenhardt

et al.

(1996, p. 326); Rossman

et al.

(1996, p. 244), De Queiroz and Lawson (1994, pp. 213-229); Rosen and Schwalbe (1988, pp. 5-7); and De Queiroz

et al.

(2002, p. 321).

Habitat and Natural History

The narrow-headed gartersnake is widely considered to be one of the most aquatic of the gartersnakes (Drummond and Marcias Garcia 1983, pp. 24, 27; Rossman

et al.

1996, p. 246). This species is strongly associated with clear, rocky streams, using predominantly pool and riffle habitat that includes cobbles and boulders (Rosen and Schwalbe 1988, pp. 33-34; Degenhardt

et al.

1996, p. 327; Rossman

et al.

1996, p. 246; Ernst and Ernst 2003, p. 417). Rossman

et al.

(1996, p. 246) also note the species has been observed using lake shoreline habitat in New Mexico. Narrow-headed gartersnakes occur at elevations from approximately 2,300 to 8,200 ft (700 to 2,500 m), inhabiting Petran Montane Conifer Forest, Great Basin Conifer Woodland, Interior Chaparral, and the Arizona Upland subdivision of Sonoran Desertscrub communities (Rosen and Schwalbe 1988, p. 33; Brennan and Holycross 2006, p. 122). An extensive evaluation of habitat use of narrow-headed gartersnakes along Oak Creek in Arizona is provided in Nowak and Santana-Bendix (2002, pp. 26-37). Rosen and Schwalbe (1988, p. 35) found narrow-headed gartersnake densities may be highest at the conjunction of cascading riffles with pools, where waters were deeper than 20 in (0.5 m) in the riffle and deeper than 40 in (1 m) in the immediately adjoining area of the pool, but more than twice the number of snakes were found in pools rather than riffles.

Where narrow-headed gartersnakes are typically found in the water, little aquatic vegetation exists (Rosen and Schwalbe 1988, p. 34). However, bank-line vegetation is an important component to suitable habitat for this species. Narrow-headed gartersnakes will usually bask in situations where a quick escape can be made, whether that is into the water or under substrate such as rocks (Fleharty 1967, p. 16). Common plant species associations include Arizona alder (

Alnus oblongifolia

) (highest correlation with occurrence of the narrow-headed gartersnake), velvet ash (

Fraxinus pennsylvanica

), willows (

Salix

ssp.), canyon grape (

Vitis arizonica

), blackberry (

Rubus

ssp.), Arizona sycamore (

Platanus wrightii

), Arizona black walnut (

Juglans major

), Freemont cottonwood (

Populus fremontii

), Gambel oak (

Quercus gambelii

), and ponderosa pine (

Pinus ponderosa

) (Rosen and Schwalbe 1988, pp. 34-35). Rosen and Schwalbe (1988, p. 35) noted that the composition of bank-side plant species and canopy structure were less important to the species' needs than was the size class of the plant species present; narrow-headed gartersnakes prefer to use shrub- and sapling-sized plants for thermoregulating (basking) at the waters' edge (Degenhardt

et al.

1996, p. 327).

Narrow-headed gartersnakes may opportunistically forage within dammed reservoirs formed by streams that are occupied habitat, such as at Wall Lake (located at the confluence of Taylor Creek, Hoyt Creek, and the East Fork Gila River) (Fleharty 1967, p. 207) and most recently at Snow Lake in 2012 (located near the confluence of Snow Creek and the Middle Fork Gila River) (Hellekson 2012b, pers. comm.) in New Mexico, but records from impoundments are rare in the literature. The species evolved in the absence of such habitat, and impoundments are generally managed as sport fisheries (Wall Lake and Snow Lake are) and

often maintain populations of harmful nonnative species that are incompatible with narrow-headed gartersnakes.

The narrow-headed gartersnake is surface-active generally between March and November (Nowak 2006, p. 16). Little information on suitable temperatures for surface activity of the narrow-headed gartersnake exists; however, it is presumed to be rather cold-tolerant based on its natural history and foraging behavior that often involves clear, cold streams at higher elevations. Along Oak Creek in Arizona, Nowak (2006, Appendix 1) found the species to be active in air temperatures ranging from 52 to 89 °F (11 to 32 °C) and water temperatures ranging from 54 to 72 °F (12 to 22 °C). Jennings and Christman (2011, pp. 12-14) found body temperatures of narrow-headed gartersnakes along the Tularosa River averaged approximately 68 °F (20 °C) during the mid-morning hours and 81 °F (27 °C) in the late afternoon during the period from late July and August. Variables that affect their body temperature include the temperature of the microhabitat used and water temperature (most predictive), but slope aspect and the surface area of cover used also influenced body temperatures (Jennings and Christman 2011, p. 13). Narrow-headed gartersnakes have a lower preferred temperature for activity as compared to other species of gartersnakes (Fleharty 1967, p. 228), which may facilitate their highly aquatic nature in cold streams.

Narrow-headed gartersnakes specialize on fish as their primary prey item (Rosen and Schwalbe 1988, p. 38; Degenhardt

et al.

1996, p. 328; Rossman

et al.

1996, p. 247; Nowak and Santana-Bendix 2002, pp. 24-25; Nowak 2006, p. 22) and are believed to be mainly visual hunters (Hibbitts and Fitzgerald 2005, p. 364), heavily dependent on visual cues when foraging based on comparative analyses among other species of gartersnakes (de Queiroz 2003, p. 381). Unlike many other species of gartersnakes that are active predators (actively crawl about in search of prey), narrow-headed gartersnakes are considered to be ambush predators (sit-and-wait method) (Brennan and Holycross 2006, p. 122; Pierce

et al.

2007, p. 8). The specific gravity (ratio of the mass of a solid object to the mass of the same volume of water) of the narrow-headed gartersnake was found to be nearly 1, which means that the snake can maintain its desired position in the water column with ease, an adaptation to facilitate foraging on the bottom of streams (Fleharty 1967, pp. 218-219). Native fish species most often associated as prey items for the narrow-headed gartersnake include Sonora sucker (

Catostomus insignis

), desert sucker (

C. clarki

), speckled dace (

Rhinichthys osculus

), roundtail chub (

Gila robusta

), Gila chub (

Gila intermedia

), and headwater chub (

Gila nigra

) (Rosen and Schwalbe 1988, p. 39; Degenhardt

et al.

1996, p. 328). Nonnative species used as prey by narrow-headed gartersnakes are most often salmonid species (trout); most commonly brown (

Salmo trutta

) and rainbow trout (

Oncorhynchus mykiss

), as these species are commonly stocked in, or near, occupied narrow-headed gartersnake habitat (Rosen and Schwalbe 1988, p. 39; Nowak 2006, pp. 22-23). Fleharty (1967, p. 223) reported narrow-headed gartersnakes eating green sunfish, but green sunfish is not considered a suitable prey item.

Several reviews (Stebbins 1985, p. 199; Deganhardt

et al.

1996, p. 328; Ernst and Ernst 2003, p. 418) state that the narrow-headed gartersnake will also prey upon frogs, tadpoles, and salamanders. Fitzgerald (1986, p. 6) referenced the Stebbins (1985) account as the only substantiated account of the species accepting something other than fish as prey, apparently as the result of finding a small salamander larvae in the stomach of an individual in Durango, Mexico. Formerly recognized as a subspecies of

Thamnophis rufipunctatus,

that individual is now recognized as

T. unilabialis

(Wood

et al.

2011, p. 3). We found an account of narrow-headed gartersnakes consuming red-spotted toads in captivity (Woodin 1950, p. 40). Despite several studies focusing on the ecology of narrow-headed gartersnakes in recent times, there are no other records of narrow-headed gartersnakes, under current taxonomic recognition, feeding on prey items other than fish. We, along with species experts, do not consider amphibians as ecologically important prey for this species based on our review of the literature.

Native predators of the narrow-headed gartersnake include birds of prey, other snakes such as kingsnakes, whipsnakes, or regal ring-necked snakes, wading birds, mergansers, belted kingfishers, raccoons, skunks, and coyotes (Rosen and Schwalbe 1988, pp. 18, 39; Brennan

et al.

2009, p. 123). Historically, large, highly predatory native fish species such as Colorado pikeminnow may have preyed upon narrow-headed gartersnakes where the species co-occurred. Native chubs (

Gila

sp.) may also prey on neonatal gartersnakes.

Sexual maturity in narrow-headed gartersnakes occurs at 2.5 years of age in males and at 2 years of age in females (Deganhardt

et al.

1996, p. 328). Narrow-headed gartersnakes are viviparous. The reproductive cycle for narrow-headed gartersnakes appears to be longer than other gartersnake species; females begin the development of follicles in early March, and gestation takes longer (Rosen and Schwalbe 1988, pp. 36-37). Female narrow-headed gartersnakes breed annually and give birth to 4 to 17 offspring from late July into early August, perhaps earlier at lower elevations (Rosen and Schwalbe 1988, pp. 35-37). Sex ratios in narrow-headed gartersnake populations can be skewed in favor of females (Fleharty 1967, p. 212).

Historical Distribution

The historical distribution of the narrow-headed gartersnake ranged across the Mogollon Rim and along its associated perennial drainages from central and eastern Arizona, southeast to southwestern New Mexico at elevations ranging from 2,300 to 8,000 ft (700 to 2,430 m) (Rosen and Schwalbe 1988, p. 34; Rossman

et al.

1996, p. 242; Holycross

et al.

2006, p. 3). The species was historically distributed in headwater streams of the Gila River subbasin that drain the Mogollon Rim and White Mountains in Arizona, and the Gila Wilderness in New Mexico; major subbasins in its historical distribution included the Salt and Verde River subbasins in Arizona, and the San Francisco and Gila River subbasins in New Mexico (Holycross

et al.

2006, p. 3). Holycross

et al.

(2006, p. 3) suspect the species was likely not historically present in the lowest reaches of the Salt, Verde, and Gila rivers, even where perennial flow persists. Numerous records for the narrow-headed gartersnake (through 1996) in Arizona are maintained in the AGFD's Heritage Database (1996b). The narrow-headed gartersnake as currently recognized does not occur in Mexico.

Current Distribution and Population Status

Where narrow-headed gartersnakes are locally abundant, they can usually be detected reliably and with significantly less effort than populations characterized as having low densities. Narrow-headed gartersnakes are well-camouflaged, secretive, and very difficult to detect in structurally complex, dense habitat where they could occur at very low population densities, which characterizes most occupied sites. Water clarity can also affect survey accuracy. We considered factors such as the date of the last known records for narrow-headed gartersnakes in an area, as well as

records of one or more native prey species in making a conclusion on species occupancy. We used all records that were dated 1980 or later because the 1980s marked the first systematic survey efforts for narrow-headed gartersnakes species across their range (see Rosen and Schwalbe (1988, entire) and Fitzgerald (1986, entire)), and the last, previous records were often dated several decades prior and may not accurately represent the likelihood for current occupation. Several areas where narrow-headed gartersnakes were known to occur have received no, or very little, survey effort in the past several decades. Variability in survey design and effort makes it difficult to compare population sizes or trends among sites and between sampling periods. Thus, for each of the sites discussed in Appendix A (available at

http://www.regulations.gov

under Docket No. FWS-R2-ES-2013-0071), we have attempted to translate and quantify search and capture efforts into comparable units (

i.e.,

person-search hours and trap-hours) and have conservatively interpreted those results. Because the presence of suitable prey species in an area may provide evidence that northern Mexican gartersnake may still persist in low density where survey data are sparse, a record of a native prey species was considered in our determination of occupancy of this species.

Population status information, based on our review of the best scientific and commercial data available, suggests that the narrow-headed gartersnake has experienced significant declines in population density and distribution along streams and rivers where it was formerly well-documented and reliably detected. Many areas where the species may occur likely rely on emigration of individuals from occupied habitat into those areas to maintain the species, provided there are no barriers to movement. Holycross

et al.

(2006) represents the most recent, comprehensive survey effort for narrow-headed gartersnakes in Arizona. Our most current information on the species' status in New Mexico comes from a species expert who is completing a graduate degree focused on the relationship between narrow-headed gartersnake populations and fish communities in the upper Gila and San Francisco river drainages (Helleckson 2012a, pers. comm.). Narrow-headed gartersnakes were detected in only 5 of 16 historical localities in Arizona and New Mexico surveyed by Holycross

et al.

(2006) in 2004 and 2005. Population densities have noticeably declined in many populations, as compared to previous survey efforts (Holycross

et al.

2006, p. 66). Holycross

et al.

(2006, pp. 66-67) compared narrow-headed gartersnake detections based on results from their effort and that of previous efforts in the same locations and found that significantly more effort is required to detect this species in areas where it was formerly robust, such as along Eagle Creek (AZ), the East Verde River (AZ), the San Francisco River (NM), the Black River (AZ), and the Blue River (AZ).

As of 2011, the only remaining narrow-headed gartersnake populations where the species could reliably be found were located at: (1) Whitewater Creek (New Mexico), (2) Tularosa River (New Mexico), (3) Diamond Creek (New Mexico), (4) Middle Fork Gila River (New Mexico), and (5) Oak Creek Canyon (Arizona). However, populations found in Whitewater Creek and the Middle Fork Gila River were likely significantly affected by New Mexico's largest wildfire in State history, the Whitewater-Baldy Complex Fire, which occurred in June 2012. In addition, salvage efforts were initiated for these two populations, which included the removal of 25 individuals from Whitewater Creek and 14 individuals from the Middle Fork Gila River before the onset of summer rains in 2012. The status of those populations has likely deteriorated as a result of subsequent declines in resident fish communities due to heavy ash and sediment flows, resulting fish kills, and the removal of snakes, but subsequent survey data have not been collected. If the Whitewater Creek and Middle Fork Gila River populations did decline as a result of these factors, only three remaining populations of this species remain viable today across their entire distribution. Such unnaturally large wildfires have become increasingly common across the Mogollon Rim of Arizona and New Mexico where the narrow-headed gartersnake historically occurred. The status of the narrow-headed gartersnake on tribal land is poorly known, due to limited survey access.

In Table 2 below, we summarize the population status of the narrow-headed gartersnake at all known localities throughout its distribution, as supported by museum records or reliable observations. For a detailed discussion that explains the rationale for site-by-site conclusions on occupancy, please see Appendix A (available at

http://www.regulations.gov

under Docket No. FWS-R2-ES-2013-0071). General rationale is provided in the introductory paragraph to this section, “Current Distribution and Population Status.”

Table 2—Current Population Status of the Narrow-Headed Gartersnake. References Cited Are Provided in Appendix A

Location

Last record

Suitable physical habitat present

Native prey species

present

Harmful nonnative species present

Population status

West Fork Gila River (NM)

2011

Yes

Yes

Yes

Likely not viable.

Middle Fork Gila River (NM)

2012

Yes

Yes

Yes

Likely not viable.

East Fork Gila River (NM)

2006

Yes

Yes

Yes

Likely not viable.

Gila River (AZ, NM)

2009

Yes

Yes

Yes

Likely not viable.

Snow Creek/Snow Lake (NM)

2012

Yes

No

Yes

Likely not viable.

Gilita Creek (NM)

2009

Yes

Yes

No

Likely not viable.

Iron Creek (NM)

2009

Yes

Yes

No

Likely not viable.

Little Creek (NM)

2010

Yes

Possible

Yes

Likely not viable.

Turkey Creek (NM)

1985

Yes

Yes

Possible

Likely not viable.

Beaver Creek (NM)

1949

Yes

Possible

Yes

Likely extirpated.

Black Canyon (NM)

2010

Yes

Yes

No

Likely not viable.

Taylor Creek (NM)

1960

Yes

No

Yes

Likely extirpated.

Diamond Creek (NM)

2011

Yes

Yes

Yes

Likely viable.

Tularosa River (NM)

2012

Yes

Yes

Yes

Likely viable.

Whitewater Creek (NM)

2012

Yes

Yes

Yes

Likely not viable.

San Francisco River (NM)

2011

Yes

Yes

Yes

Likely not viable.

South Fork Negrito Creek (NM)

2011

Yes

Possible

Yes

Likely not viable.

Blue River (AZ)

2007

Yes

Yes

Yes

Likely not viable.

Dry Blue Creek (AZ, NM)

2010

Yes

Possible

Yes

Likely not viable.

Campbell Blue Creek (AZ, NM)

2010

Yes

Possible

Yes

Likely not viable.

Saliz Creek (NM)

2012

Yes

Possible

Yes

Likely not viable.

Eagle Creek (AZ)

1991

Yes

Yes

Yes

Likely not viable.

Black River (AZ)

2009

Yes

Yes

Yes

Likely not viable.

White River (AZ)

1986

Yes

Yes

Possible

Likely not viable.

Diamond Creek (AZ)

1986

Yes

Possible

Possible

Likely not viable.

Tonto Creek (tributary to Big Bonita Creek, AZ)

1915

Yes

Possible

Possible

Likely extirpated.

Canyon Creek (AZ)

1991

Yes

Yes

No

Likely not viable.

Upper Salt River (AZ)

1985

Yes

Yes

Yes

Likely not viable.

Cibeque Creek (AZ)

1991

Yes

Yes

Possible

Likely not viable.

Carrizo Creek (AZ)

1997

Yes

Yes

Possible

Unreliably detected.

Big Bonito Creek (AZ)

1957

Yes

Yes

Yes

Likely extirpated.

Haigler Creek (AZ)

Early 1990s

Yes

Yes

Yes

Likely not viable.

Houston Creek (AZ)

2005

Yes

Yes

Yes

Likely not viable.

Tonto Creek (tributary to Salt River, AZ)

2005

Yes

Yes

Yes

Likely not viable.

Deer Creek (AZ)

1995

No

No

No

Likely extirpated.

Upper Verde River (AZ)

2012

Yes

Yes

Yes

Likely not viable.

Oak Creek (AZ)

2012

Yes

Yes

Yes

Likely viable.

East Verde River (AZ)

1992

Yes

Yes

Yes

Likely not viable.

“Possible” means there were no conclusive data found.

“Likely extirpated” means the last record for an area pre-dated 1980 and existing threats suggest the species is likely extirpated. “Likely not viable” means there is a post-1980 record for the species, it is not reliably found with minimal to moderate survey effort, and threats exist which suggest the population may be low density or could be extirpated, but there is insufficient evidence to confirm extirpation. “Likely viable” means that the species is reliably found with minimal to moderate survey effort and the population is generally considered viable.

Table 2 lists the 38 known localities for narrow-headed gartersnakes throughout their range. Appendix A (available at

http://www.regulations.gov

under Docket No. FWS-R2-ES-2013-0071) discusses such considerations as the physical condition of habitat, the composition of the aquatic biological community, the existence of significant threats, and the length of time since the last known observation of the species in presenting rationale for determining occupancy status at each locality. We have concluded that in as many as 29 of 38 known localities (76 percent), the narrow-headed gartersnake population is likely not viable and may exist at low population densities that could be threatened with extirpation or may already be extirpated but survey data are lacking in areas where access is restricted. In most localities where the species may occur at low population densities, existing survey data are insufficient to conclude extirpation. As of 2012, narrow-headed gartersnake populations are considered likely viable in 3 localities (8 percent) where individuals are reliable detected. As displayed in Table 2, harmful nonnative species are a concern for almost every narrow-headed gartersnake population throughout their range. The ramifications of this are significant because of the effect these harmful nonnative species have on the resident native fish communities and the fact that this species is a specialized, fish-only predator. We discuss this and other important factors that have contributed to the decline of narrow-headed gartersnakes throughout their range in our threats analysis below.

Summary of Factors Affecting the Species

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

In the following threats analysis, we treat both gartersnake species in a combined discussion because of partially overlapping ranges, similar natural histories, similar responses to threats, and the fact that many threats are shared in common throughout their ranges.

The Weakened Status of Native Aquatic Communities

Riparian and aquatic communities in both the United States and Mexico have been significantly impacted by a shift in species' composition, from one of primarily native fauna, to one being increasingly dominated by an expanding assemblage of nonnative animal species. Many of these nonnative species have been intentionally or accidentally introduced, including crayfish, bullfrogs, and nonnative, spiny-rayed fish. Harmful nonnative species have been introduced or have spread into new areas through a variety of mechanisms, including intentional and accidental releases, sport stocking, aquaculture, aquarium releases, and bait-bucket release.

The occurrence of harmful nonnative species, such as the bullfrog, the northern (virile) crayfish (

Orconectes virilis

), red swamp crayfish (

Procambarus clarkii

), and numerous species of nonnative, spiny-rayed fish,

has contributed to rangewide declines in both species of gartersnake, and continues to be the most significant threat to the northern Mexican and narrow-headed gartersnakes, and to their prey base, as a result of direct predation, competition, and modification of habitat as evidenced in a broad body of literature, the most recent of which extends from 1985 to the present (Meffe 1985, pp. 179-185; Propst

et al.

1986, pp. 14-31, 82; 1988, p. 64; 2009, pp. 5-17; Minckley 1987, pp. 2, 16; 1993, pp. 7-13; Rosen and Schwalbe 1988, pp. 28, 32; 1997, p. 1; Bestgen and Propst 1989, pp. 409-410; Clarkson and Rorabaugh 1989, pp. 531, 535; Papoulias

et al.

1989, pp. 77-80; Marsh and Minckley 1990, p. 265; Jakle 1992, pp. 3-5; 1995, pp. 5-7; ASU 1994, multiple reports; 1995, multiple reports; 2008, multiple reports; Stefferud and Stefferud 1994, p. 364; Douglas

et al.

1994, pp. 9-19; Rosen

et al.

1995, pp. 257-258; 1996b, pp. 2, 11-13; 2001, p. 2; Springer 1995, pp. 6-10; Degenhardt

et al.

1996, p. 319; Fernandez and Rosen 1996, pp. 8, 23-27, 71, 96; Richter

et al.

1997, pp. 1089, 1092; Weedman and Young 1997, pp. 1, Appendices B, C; Inman

et al.

1998, p. 17; Rinne

et al.

1998, pp. 4-6; 2004, pp. 1-2; Jahrke and Clark 1999, pp. 2-7; Minckley

et al.

2002, pp. 696; Nowak and Santana-Bendix 2002, Table 3; Propst 2002, pp. 21-25; DFT 2003, pp. 1-3, 5-6, 19; 2004, pp. 1-2, 4-5, 10, Table 1; 2006, pp. iii, 25; Marsh

et al.

2003, p. 667; Bonar

et al.

2004, pp. 13, 16-21; Rinne 2004, pp. 1-2; Clarkson

et al.

2005, p. 20; 2008, pp. 3-4; Fagan

et al.

2005, pp. 34, 34-41; Knapp 2005, pp. 273-275; Olden and Poff 2005, pp. 82-87; AGFD 2006, p. 83; Turner 2007, p. 41; Holycross

et al.

2006, pp. 13-15; Brennan and Holycross 2006, p. 123; Brennan 2007, pp. 5, 7; Turner and List 2007, p. 13; USFWS 2007, pp. 22-23; Burger 2008, p. 4; Caldwell 2008a, 2008b; Duifhuis Rivera

et al.

2008, p. 479, Jones 2008b; d'Orgeix 2008; Haney

et al.

2008, p. 59; Luja and Rodríguez-Estrella 2008, pp. 17-22; Probst

et al.

2008, pp. 1242-1243; Rorabaugh 2008a, p. 25; USFS 2008; Wallace

et al.

2008, pp. 243-244; Witte

et al.

2008, p. 1; Bahm and Robinson 2009a, pp. 2-6; 2009b, pp. 1-4; Brennan and Rosen 2009, pp. 8-9; Karam

et al.

2009; pp. 2-3; Minckley and Marsh 2009, pp. 50-51; Paroz

et al.

2009, pp. 12, 18; Robinson and Crowder 2009, pp. 3-5; Pilger

et al.

2010, pp. 311-312; Stefferud

et al.

2011, pp. 11-12; C. Akins 2012, pers. comm.; Young and Boyarski 2013, pp. 159-160; Emmons and Nowak 2013, p. 5).

The Decline of the Gartersnake Prey Base

The documented decline of the northern Mexican and narrow-headed gartersnakes was typically subsequent to the declines in their prey base (native amphibian and fish populations). These declines in prey base result from predation following the establishment of nonnative bullfrogs, crayfish, and numerous species of nonnative, spiny-rayed fish as supported by an extensive body of literature referenced immediately above.

Northern Mexican and narrow-headed gartersnakes appear to be particularly vulnerable to the loss of native prey species (Rosen and Schwalbe 1988, pp. 20, 44-45). Rosen

et al.

(2001, pp. 10, 13, 19) examined this issue in detail with respect to the northern Mexican gartersnake, and proposed two reasons for its decline following a loss of, or decline in, the native prey base: (1) The species is unlikely to increase foraging efforts at the risk of increased predation; and (2) the species needs adequate food on a regular basis to maintain its weight and health. If forced to forage more often for smaller prey items, a reduction in growth and reproductive rates can result (Rosen

et al.

2001, pp. 10, 13). Rosen

et al.

(2001, p. 22) concluded that the presence and expansion of nonnative predators (mainly bullfrogs, crayfish, and green sunfish (

Lepomis cyanellus

)) is the primary cause of decline in northern Mexican gartersnakes and their prey in southeastern Arizona. In another example, Drummond and Marcias Garcia (1983, pp. 25, 30) found that Mexican gartersnakes fed primarily on frogs, and functioned as a local specialist in that regard. When frogs became unavailable, the species simply ceased major foraging activities. This led the author to conclude that frog abundance is probably the most important correlate, and main determinant, of foraging behavior in this species. Alternatively, terrestrial prey species were consumed, but the gartersnakes were never documented as having these prey items as a major dietary component, even when the gartersnakes were in dire need (Drummond and Marcias Garcia 1983, p. 37).

With respect to narrow-headed gartersnakes, the relationship between harmful nonnative species, a declining prey base, and gartersnake populations is clearly depicted in one population along Oak Creek. Nowak and Santana-Bendix (2002, Table 3) found a clear partition in the distribution of nonnative, spiny-rayed fish and soft-rayed fish in the vicinity of Midgely Bridge, where nonnative, spiny-rayed fish increased in abundance in the downstream direction and soft-rayed fish increased in abundance in the upstream direction. These fish community distributions closely parallel that of narrow-headed gartersnakes along Oak Creek, where gartersnake populations increase in density in the upstream direction and decrease notably in the downstream direction (Nowak and Santana-Bendix 2002, p. 23). Numerous historical records for narrow-headed gartersnakes document the species in the lower reach of Oak Creek, but the species is currently rarely detected in this reach of Oak Creek (Nowak and Santana-Bendix 2002, pp. 13-14), providing evidence of the decline of narrow-headed gartersnakes in the presence of nonnative, spiny-rayed fish.

Fish

—Northern Mexican and narrow-headed gartersnakes can successfully use nonnative, soft-rayed fish species as prey, including mosquitofish, red shiner, and introduced trout (

Salmo

sp.) (Nowak and Santana-Bendix 2002, pp. 24-25; Holycross

et al.

2006, p. 23). However, all other nonnative species, most notably the spiny-rayed fish, are not considered prey species for northern Mexican or narrow-headed gartersnakes and, in addition, are known to prey on neonatal and juvenile gartersnakes. Nowak and Santana-Bendix (2002, p. 24) propose two hypotheses regarding the reluctance of narrow-headed gartersnakes to prey on nonnative, spiny-rayed fish: (1) The laterally-compressed shape and presence of sharp, spiny dorsal spines present a choking hazard to gartersnakes that has been observed to be fatal; and (2) nonnative, spiny-rayed fish tend to occupy the middle and upper zones in the water column, while narrow-headed gartersnakes typically hunt along the bottom (where native fish tend to occur). As a result, nonnative, spiny-rayed fish may be largely ecologically unavailable as prey. It is likely the shape and presence of sharp, spiny dorsal spines on these nonnative fish species also present a choking hazard to both northern Mexican and narrow-headed gartersnakes.

Nonnative, spiny-rayed fish invasions can indirectly affect the health, maintenance, and reproduction of northern Mexican and narrow-headed gartersnakes by altering their foraging strategy and compromising foraging success. Rosen

et al.

(2001, p. 19), in addressing the northern Mexican gartersnake, proposed that an increase in energy expended in foraging, coupled by the reduced number of small to

medium-sized prey fish available, results in deficiencies in nutrition, affecting growth and reproduction. This occurs because energy is allocated to maintenance and the increased energy costs of intense foraging activity, rather than to growth and reproduction. In contrast, a northern Mexican gartersnake diet that includes both fish and amphibians, such as leopard frogs, reduces the necessity to forage at a higher frequency, allowing metabolic energy gained from larger prey items to be allocated instead to growth and reproductive development. Myer and Kowell (1973, p. 225) experimented with food deprivation in common gartersnakes, and found significant reductions in lengths and weights of juvenile snakes that were deprived of regular feedings versus the control group that were fed regularly at natural frequencies. Reduced foraging success of both northern Mexican and narrow-headed gartersnakes means that individuals are likely to become vulnerable to effects from starvation, which may increase mortality rates of juveniles and, consequently, affect recruitment.

Northern Mexican gartersnakes have a more varied diet than narrow-headed gartersnakes. We are not aware of any studies that have addressed the direct relationship between prey base diversity and northern Mexican gartersnake recruitment and survivorship. However, Krause and Burghardt (2001, pp. 100-123) discuss the benefits and costs that may be associated with diet variability in the common gartersnake (

Thamnophis sirtalis

), an ecologically similar species to the northern Mexican gartersnake. Foraging for mixed-prey species may impede predator learning, as compared to specialization, on a certain prey species, but may also provide long-term benefits (Krause and Burghardt 2001, p. 101). Krause and Burghardt (2001, p. 112) stated that varied predatory experience played an important role in the feeding abilities of gartersnakes through the first 8 months of age. These data suggest that a varied prey base might also be important for neonatal and juvenile northern Mexican gartersnakes (also a species with a varied diet) and that decreases in the diversity of the prey base during the young age classes might adversely affect the ability of individuals to capture prey throughout their lifespan, in addition to the more obvious effects of reduced prey availability.

A wide variety of native fish species, now listed as endangered, threatened, or candidates for listing, were historically primary prey species for northern Mexican and narrow-headed gartersnakes (Rosen and Schwalbe 1988, pp. 18, 39). Aquatic habitat destruction and modification is often considered a leading cause for the decline in native fish in the southwestern United States. However, Marsh and Pacey (2005, p. 60) predict that despite the significant physical alteration of aquatic habitat in the southwest, native fish species could not only complete all of their life functions but could flourish in these altered environments, but for the presence of (harmful) nonnative fish species, as supported by a “substantial and growing body of evidence derived from case studies.” Northern Mexican and narrow-headed gartersnakes depend on native fish as a principle part of their prey base, although nonnative, soft-rayed fish are also common prey items where they overlap in distribution with these gartersnakes (Nowak and Santana-Bendix 2002, pp. 24-25; Holycross

et al.

2006, p. 23). Nonnative, spiny-rayed fish compete with northern Mexican and narrow-headed gartersnakes for prey. In their extensive surveys, Rosen and Schwalbe (1988, p. 44) only found narrow-headed gartersnakes in abundance where native fish species predominated, but did not find them abundant in the presence of robust nonnative, spiny-rayed fish populations. Minckley and Marsh (2009, pp. 50-51) found nonnative fishes to be the single-most significant factor in the decline of native fish species and also their primary obstacle to recovery. Of the 48 conterminous States in the United States, Arizona has the highest proportion of nonnative fish species (66 percent) represented by approximately 68 species of nonnative fish (Turner and List 2007, p. 13).

Collier

et al.

(1996, p. 16) note that interactions between native and nonnative fish have significantly contributed to the decline of many native fish species from direct predation and, indirectly, from competition (which has adversely affected the prey base for northern Mexican and narrow-headed gartersnakes). The AGFD considers native fish in Arizona as the most threatened taxa among the State's native species, largely as a result of predation and competition with nonnative species (AGFD 2006, p. 83). Holycross

et al.

(2006, pp. 52-61) documented significantly depressed or extirpated native fish prey bases for northern Mexican and narrow-headed gartersnakes along the Mogollon Rim in Arizona and New Mexico. Rosen

et al.

(2001, Appendix I) documented the decline of several native fish species in several locations visited in southeastern Arizona, further affecting the prey base of northern Mexican gartersnakes in that area.

Stocked for sport, forage, or biological control, nonnative fishes have been shown to become invasive where released, do not require natural flow regimes, and tend to be more phylogenetically advanced than native species (Kolar

et al.

2003, p. 9) which contributed to their expansion in the Gila River basin. Harmful nonnative fish species tend to be nest-builders and actively guard their young which may provide them another ecological advantage over native species which are broadcast spawners and provide no parental care to their offspring (Marsh and Pacey 2005, p. 60). It is therefore likely that recruitment and survivorship is greater in nonnative species than native species where they overlap, providing them with an ecological advantage. Table 2-1 in Kolar

et al.

(2003, p. 10) provides a map depicting the high degree of overlap in the distribution of native and nonnative fishes within the Gila River basin of Arizona and New Mexico as well as watersheds thought to be dominated by nonnative fish species. The widespread decline of native fish species from the arid southwestern United States and Mexico has resulted largely from interactions with nonnative species and has been captured in the listing rules of 13 native species listed under the Act, and whose historical ranges overlap with the historical distribution of northern Mexican and narrow-headed gartersnakes. Native fish species that were likely prey species for these gartersnakes and are now listed under the Act, include the bonytail chub (

Gila elegans,

45 FR 27710, April 23, 1980), Yaqui catfish (

Ictalurus pricei,

49 FR 34490, August 31, 1984), Yaqui chub (

Gila purpurea,

49 FR 34490, August 31, 1984), Yaqui topminnow (

Poeciliopsis occidentalis sonoriensis,

32 FR 4001, March 11, 1967), beautiful shiner (

Cyprinella formosa,

49 FR 34490, August 31, 1984), humpback chub (

Gila cypha,

32 FR 4001, March 11, 1967), Gila chub (

Gila intermedia,

70 FR 66663, November 2, 2005), Colorado pikeminnow (

Ptychocheilus lucius,

32 FR 4001, March 11, 1967), spikedace (

Meda fulgida,

77 FR 10810, February 23, 2012), loach minnow (

Tiaroga cobitis,

77 FR 10810, February 23, 2012), razorback sucker (

Xyrauchen texanus,

56 FR 54957, October 23, 1991), desert pupfish (

Cyprinodon macularius,

51 FR 10842, March 31, 1986), and Gila topminnow (

Poeciliopsis occidentalis,

32 FR 4001, March 11, 1967). In total, within Arizona, 19 of 31 (61 percent) native

fish species are listed under the Act. Arizona ranks the highest of all 50 States in the percentage of native fish species with declining trends (85.7 percent) and New Mexico ranks sixth (48.1 percent) (Stein 2002, p. 21; Warren and Burr 1994, p. 14). Recovery of native fishes in the Southwest has been fraught with complicating factors, both natural and sociopolitical, which have presented significant challenges to the recovery of many imperiled native fish species (Minckley and Marsh 2009, pp. 52-53), including many that are important prey species for the northern Mexican and narrow-headed gartersnakes.

In an evolutionary context, many native fishes co-evolved with very few predatory fish species, whereas most of the nonnative species co-evolved with many predatory species (Clarkson

et al.

2005, p. 21). A contributing factor to the decline of native fish species cited by Clarkson

et al.

(2005, p. 21) is that most of the nonnative species evolved behaviors, such as nest guarding, to protect their offspring from these many predators, while native species are generally broadcast spawners that provide no parental care. In the presence of nonnative species, the reproductive behaviors of native fish fail to allow them to compete effectively with the nonnative species, and, as a result, the viability of native fish populations is reduced.

Olden and Poff (2005, p. 75) stated that environmental degradation and the proliferation of nonnative fish species threaten the highly localized and unique fish faunas of the American Southwest. The fastest expanding nonnative species are red shiner (

Cyprinella lutrensis

), fathead minnow (

Pimephales promelas

), green sunfish, largemouth bass (

Micropterus salmoides

), western mosquitofish, and channel catfish (

Ictalurus punctatus

). These species are considered to be the most invasive in terms of their negative impacts on native fish communities (Olden and Poff 2005, p. 75). Many nonnative fishes, in addition to those listed immediately above, including yellow and black bullheads (

Ameiurus

sp.), flathead catfish (

Pylodictis olivaris

), and smallmouth bass (

Micropterus dolomieu

), have been introduced into formerly and currently occupied northern Mexican or narrow-headed gartersnake habitat and are predators on these species and their prey (Bestgen and Propst 1989, pp. 409-410; Marsh and Minckley 1990, p. 265; Sublette

et al.

1990, pp. 112, 243, 246, 304, 313, 318; Abarca and Weedman 1993, pp. 6-12; Stefferud and Stefferud 1994, p. 364; Weedman and Young 1997, pp. 1, Appendices B, C; Rinne

et al.

1998, pp. 3-6; Voeltz 2002, p. 88; Bonar

et al.

2004, pp. 1-108; Fagan

et al.

2005, pp. 34, 38-39, 41; Probst

et al.

2008, pp. 1242-1243). Nonnative, spiny-rayed fish species, such as flathead catfish, may be especially dangerous to narrow-headed gartersnake populations through competition and direct predation, because they are primarily piscivorous (fish-eating) (Pilger

et al.

2010, pp. 311-312), have large mouths, and have a tendency to occur along the stream bottom, where narrow-headed gartersnakes principally forage.

Rosen

et al.

(2001, Appendix I) and Holycross

et al.

(2006, pp. 15-51) conducted large-scale surveys for northern Mexican gartersnakes in southeastern and central Arizona and narrow-headed gartersnakes in central and east-central Arizona, and documented the presence of nonnative fish at many locations. Holycross

et al.

(2006, pp. 14-15) found nonnative fish species in 64 percent of the sample sites in the Agua Fria subbasin, 85 percent of the sample sites in the Verde River subbasin, 75 percent of the sample sites in the Salt River subbasin, and 56 percent of the sample sites in the Gila River subbasin. In total, nonnative fish were observed at 41 of the 57 sites surveyed (72 percent) across the Mogollon Rim (Holycross

et al.

2006, p. 14). Entirely native fish communities were detected in only 8 of 57 sites surveyed (14 percent) (Holycross

et al.

2006, p. 14). It is well documented that nonnative fish have now infiltrated the majority of aquatic communities in the southwestern United States as depicted in Tables 1 and 2, above, as well as in Appendix A (available at

http://www.regulations.gov

under Docket No. FWS-R2-ES-2013-0071).

Several authors have identified both the presence of nonnative fish as well as their deleterious effects on native species within Arizona. Many areas have seen a shift from a predominance of native fishes to a predominance of nonnative fishes. On the upper Verde River, native species dominated the total fish community at greater than 80 percent from 1994 to 1996, before dropping to approximately 20 percent in 1997 and 19 percent in 2001. At the same time, three nonnative species increased in abundance between 1994 and 2000 (Rinne

et al.

2004, pp. 1-2). In an assessment of the Verde River, Bonar

et al.

(2004, p. 57) found that in the Verde River mainstem, nonnative fishes were approximately 2.6 times more dense per unit volume of river than native fishes, and their populations were approximately 2.8 times that of native fishes per unit volume of river. Haney

et al.

(2008, p. 61) declared the northern Mexican gartersnake as nearly lost from the Verde River but also suggested that diminished river flow may be an important factor. Similar changes in the dominance of nonnative fishes have occurred on the Middle Fork Gila River, with a 65 percent decline of native fishes between 1988 and 2001 (Propst 2002, pp. 21-25). Abarca and Weedman (1993, pp. 6-12) found that the number of nonnative fish species was twice the number of native fish species in Tonto Creek in the early 1990s, with a stronger nonnative species influence in the lower reaches, where the northern Mexican gartersnake is considered to still occur, and Burger (2008, p. 8) confirmed their continued existence there. Surveys in the Salt River above Lake Roosevelt indicate a decline of roundtail chub and other natives with an increase in flathead and channel catfish numbers (Voeltz 2002, p. 49).

In New Mexico, nonnative fish have been identified as the main cause for declines observed in native fish populations (Voeltz 2002, p. 40; Probst

et al.

2008, pp. 1242-1243). Fish experts from the U.S. Forest Service, U.S. Bureau of Reclamation, U.S. Bureau of Land Management (BLM), University of Arizona, Arizona State University, the Nature Conservancy, and others declared the native fish fauna of the Gila River basin to be critically imperiled, and they cite habitat destruction and nonnative species as the primary factors for the declines. They call for the control and removal of nonnative fish as an overriding need to prevent the decline, and ultimate extinction, of native fish species within the basin (DFT 2003, p. 1). In some areas, nonnative fishes may not dominate the system, but their abundance has increased. This is the case for the Cliff-Gila Valley area of the Gila River, where nonnative fishes increased from 1.1 percent to 8.5 percent, while native fishes declined steadily over a 40-year period (Propst

et al.

1986, pp. 27-32). At the Redrock and Virden valleys on the Gila River, the relative abundance in nonnative fishes in the same time period increased from 2.4 percent to 17.9 percent (Propst

et al.

1986, pp. 32-34). Four years later, the relative abundance of nonnative fishes increased to 54.7 percent at these sites (Propst

et al.

1986, pp. 32-36). The percentage of nonnative fishes increased by almost 12 percent on the Tularosa River between 1988 and 2003, while on the East Fork Gila River, nonnative fishes increased to 80.5 percent relative abundance in 2003 (Propst 2005, pp. 6-7, 23-24).

Nonnative fishes are also considered a management issue in other areas including Eagle Creek, the San Pedro River, West Fork Gila River, and to a lesser extent, the Blue River.

In addition to harmful nonnative species, various parasites may affect native fish species that are prey for northern Mexican and narrow-headed gartersnakes. Asian tapeworm was introduced into the United States with imported grass carp (

Ctenopharyngodon idella

) in the early 1970s. It has since become well established in areas throughout the southwestern United States. The definitive host in the life cycle of Asian tapeworm is a cyprinid fish (carp or minnow), and therefore it is a potential threat to native cyprinids in Arizona and New Mexico. The Asian tapeworm adversely affects fish health by impeding the digestion of food as it passes through the digestive track. Emaciation and starvation of the host can occur when large enough numbers of worms feed off the fish directly. An indirect effect is that weakened fish are more susceptible to infection by other pathogens. Asian tapeworm invaded the Gila River basin and was found during the Central Arizona Project's fall 1998 monitoring in the Gila River at Ashurst-Hayden Dam. It has also been confirmed from Bonita Creek in 2010 (USFWS National Wild Fish Health Survey 2010). This parasite can infect many species of fish and is carried into new areas along with nonnative fishes or native fishes from contaminated areas.

Another parasite (

Ichthyophthirius multifiliis

) (Ich) usually occurs in deep waters with low flow and is a potential threat to native fish. Ich has occurred in some Arizona streams, probably encouraged by high temperatures and crowding as a result of drought. This parasite was observed being transmitted on the Sonora sucker (

Catostomus insignis

), although it does not appear to be host-specific and could be transmitted by other species (Mpoame 1982, p. 46). It has been found on desert and Sonoran suckers, as well as roundtail chub (Robinson

et al.

1998, p. 603), which are important prey species for the northern Mexican and narrow-headed gartersnakes. This parasite becomes embedded under the skin and within the gill tissues of infected fish. When Ich matures, it leaves the fish, causing fluid loss, physiological stress, and sites that are susceptible to infection by other pathogens. If Ich is present in large enough numbers, it can also impact respiration because of damaged gill tissue.

Anchor worm (

Lernaea cyprinacea

), an external parasite, is unusual in that it has little host specificity, infecting a wide range of fishes and amphibians. Infection by this parasite has been known to kill large numbers of fish due to tissue damage and secondary infection of the attachment site (Hoffnagle and Cole 1999, p. 24). Presence of this parasite in the Gila River basin is a threat to native fishes. In July 1992, the BLM found anchor worms in Bonita Creek. They have also been documented in the Verde River (Robinson

et al.

1998, pp. 599, 603-605).

The yellow grub (

Clinostomum marginatum)

is a parasitic, larval flatworm that appears as yellow spots on the body and fins of a fish. Because the intermediate host is a bird and therefore highly mobile, yellow grubs are easily spread. When yellow grubs infect a fish, they penetrate the skin and migrate into its tissues, causing damage and potentially hemorrhaging. Damage from one yellow grub may be minimal, but in greater numbers, yellow grubs can kill fish (Maine Department of Inland Fisheries and Wildlife 2002a, p. 1). Yellow grubs occur in many areas in Arizona and New Mexico, including Oak Creek (Mpoame and Rinne 1983, pp. 400-401), the Salt River (Amin 1969, p. 436; Bryan and Robinson 2000, p. 19), the Verde River (Bryan and Robinson 2000, p. 19), and Bonita Creek (Robinson 2011, pers. comm.).

The black grub (

Neascus

spp.), also called black spot, is a parasitic larval fluke that appears as black spots on the skin, tail base, fins, and musculature of a fish. When an intermediate life stage of black grubs migrates into the tissues of a fish they are called “cercaria.” The damage caused by one cercaria is negligible, but in greater numbers they may kill a fish (Lane and Morris 2000, pp. 2-3; Maine Department of Inland Fisheries and Wildlife 2002b, p. 1). Black grubs are present in the Verde River (Robinson

et al.

1998, p. 603; Bryan and Robinson 2000, p. 21), and are prevalent in the San Francisco River in New Mexico (Paroz 2011, pers. comm.).

To date, we have no information on the effect of parasite infestation in native fish on both gartersnake populations.

The Decline of Native Fish Communities in Mexico

—The first tabulations of freshwater fish species at risk in Mexico occurred in 1961, when 11 species were identified as being at risk (Contreras-Balderas

et al.

2003, p. 241). As of 2003, of the 506 species of freshwater fish recorded in Mexico, 185 (37 percent) have been listed by the Mexican Federal Government as either endangered, facing extinction, under special protection, or likely extinct (Alvarez-Torres

et al.

2003, p. 323), almost a 17-fold increase in slightly over four decades; 25 species are believed to have gone extinct (Contreras-Balderas

et al.

2003, p. 241). In the lower elevations of Mexico, within the distribution of the northern Mexican gartersnake, there are approximately 200 species of native freshwater fish documented, with 120 native species under some form of threat and an additional 15 that have gone extinct (Contreras-Balderas and Lozano 1994, pp. 383-384). The Fisheries Law in Mexico empowered the country's National Fisheries Institute to compile and publish the National Fisheries Chart in 2000, which found that Mexico's fish fauna has seriously deteriorated as a result of environmental impacts (pollution), water basin degradation (dewatering, siltation), and the introduction of nonnative species (Alvarez-Torres

et al.

2003, pp. 320, 323). The National Fisheries Chart is regarded as the first time the Mexican government has openly revealed the status of its freshwater fisheries and described their management policies (Alvarez-Torres

et al.

2003, pp. 323-324).

Industrial, municipal, and agricultural water pollution, dewatering of aquatic habitat, and the proliferation nonnative species are widely considered to be the greatest threats to freshwater ecosystems in Mexico (Branson

et al.

1960, p. 218; Conant 1974, pp. 471, 487-489; Miller

et al.

1989, pp. 25-26, 28-33; 2005, pp. 60-61; DeGregorio 1992, p. 60; Contreras Balderas and Lozano 1994, pp. 379-381; Lyons

et al.

1995, p. 572; 1998, pp. 10-12; va Landa

et al.

1997, p. 316; Mercado-Silva

et al.

2002, p. 180; Contreras-Balderas

et al.

2003, p. 241; Domínguez-Domínguez

et al.

2007, Table 3). A shift in land use policies in Mexico to encourage free market principles in rural, small-scale agriculture has been found to promote land use practices that threaten local biodiversity (Ortega-Huerta and Kral 2007, p. 2; Randall 1996, pp. 218-220; Kiernan 2000, pp. 13-23). These threats have been documented throughout the distribution of the northern Mexican gartersnake in Mexico and are best represented in the scientific literature in the context of fisheries studies. Contreras-Balderas

et al.

(2003, pp. 241, 243) named Chihuahua (46 species), Coahuila (35 species), Sonora (19 species), and Durango (18 species) as Mexican states that had some of the most reports of freshwater fish species at risk. These states are all within the distribution of the northern Mexican gartersnake, indicating an overlapping trend of declining prey bases and

threatened ecosystems within the range of the northern Mexican gartersnake in Mexico. Contreras-Balderas

et al.

(2003, Appendix 1) found various threats to be adversely affecting the status of freshwater fish and their habitat in several states in Mexico: (1) Habitat reduction or alteration (Sonora, Chihuahua, Durango, Coahuila, San Luis Potosí, Jalisco, Guanajuato); (2) water depletion (Chihuahua, Durango, Coahuila, Sonora, Guanajuato, Jalisco, San Luis Potosí); (3) harmful nonnative species (Durango, Chihuahua, Coahuila, San Luis Potosí, Sonora, Veracruz); and (4) pollution (México, Jalisco, Chihuahua, Coahuila, Durango). Within the states of Chihuahua, Durango, Coahuila, Sonora, Jalisco, and Guanajuato, water depletion is considered serious, with entire basins having been dewatered, or conditions have been characterized as “highly altered” (Contreras-Balderas

et al.

2003, Appendix 1). All of the Mexican states with the highest numbers of fish species at risk are considered arid, a condition hastened by increasing desertification (Contreras-Balderas

et al.

2003, p. 244).

Aquaculture and Nonnative Fish Proliferation in Mexico

—Nonnative fish compete with and prey upon northern Mexican gartersnakes and their native prey species. The proliferation of nonnative fish species throughout Mexico happened mainly by natural dispersal, intentional stockings, and accidental breaches of artificial or constructed barriers by nonnative fish. Lentic water bodies such as lakes, reservoirs, and ponds are often used for flood control, agricultural purposes, and most commonly to support commercial fisheries. The most recent estimates indicate that Mexico has 13,936 of such water bodies, where approximately 96 percent are between 2.47-247 acres (1-100 hectares) and approximately half are artificial (Sugunan 1997, Table 8.3; Alvarez-Torres

et al.

2003, pp. 318, 322). Areas where these landscape features are most prevalent occur within the distribution of the northern Mexican gartersnake. For example, Jalisco and Zacatecas are listed as two of four states with the highest number of reservoirs, and Chihuahua is one of two states known for a high concentration of lakes (Sugunan 1997, Section 8.4.2). Based on the data presented in Sugunan (1997, Table 8.5), a total of 422 dammed reservoirs are located within the 16 Mexican states where the northern Mexican gartersnake is thought to occur. Mercado-Silva

et al.

(2006, p. 534) found that within the state of Guanajuato, “Practically all streams and rivers in the [Laja] basin are truncated by reservoirs or other water extraction and storage structures.” On the Laja River alone, there are two major reservoirs and a water diversion dam; 12 more reservoirs are located on its tributaries (Mercado-Silva

et al.

2006, p. 534). As a consequence of dam operations, the main channel of the Laja remains dry for extensive periods of time (Mercado-Silva

et al.

2006, p. 541). The damming and modification of the lower Colorado River in Mexico, where the northern Mexican gartersnake occurred, has facilitated the replacement of the entire native fishery with nonnative species (Miller

et al.

2005, p. 61). Each reservoir created by a dam is either managed as a nonnative commercial fishery or has become a likely source population of nonnative species, which have naturally or artificially colonized the reservoir, dispersed into connected riverine systems, and damaged native aquatic communities.

Mexico, as with other developing countries, depends in large part on freshwater commercial fisheries as a source of protein for both urbanized and rural human populated areas. Commercial and subsistence fisheries rely heavily on introduced, nonnative species in the largest freshwater lakes (Soto-Galera

et al.

1999, p. 133) down to rural, small ponds (Tapia and Zambrano 2003, p. 252). At least 87 percent of the species captured or cultivated in inland fisheries of Mexico from 1989-1999 included tilapia, common carp, channel catfish, trout, and black bass (

Micropterus

sp.), all of which are nonnative (Alvarez-Torres

et al.

2003, pp. 318, 322). In fact, the northern and central plateau region of Mexico (which comprises most of the distribution of the northern Mexican gartersnake's distribution in Mexico) is considered ideal for the production of harmful, predatory species such as bass and catfish (Sugunan 1997, Section 8.3). Largemouth bass are now produced and stocked in reservoirs and lakes throughout the distribution of the northern Mexican gartersnake (Sugunan 1997, Section 8.8.1). The Secretariat for Environment, Natural Resources and Fisheries, formed in 1995 and known as SEMARNAP, is the Mexican federal agency responsible for management of the country's environment and natural resources. SEMARNAP dictates the stocking rates of nonnative species into the country's lakes and reservoirs. For example, the permitted stocking rate for largemouth bass in Mexico is one fish per square meter in large reservoirs (Sugunan 1997, Table 8.8); therefore, a 247-acre (100-ha) reservoir could be stocked with 1,000,000 largemouth bass. The common carp, the subject of significant aquaculture investment since the 1960s in Mexico, is known for altering aquatic habitat and consuming the eggs and fry of native fish species, and is now established in 95 percent of Mexico's freshwater systems (Tapia and Zambrano 2003, p. 252).

Basins in northern Mexico, such as the Rio Yaqui, have been found to be significantly compromised by harmful nonnative fish species. Unmack and Fagan (2004, p. 233) compared historical museum collections of nonnative fish species from the Gila River basin in Arizona and the Yaqui River basin in Sonora, Mexico, to gain insight into the trends in distribution, diversity, and abundance of nonnative fishes in each basin over time. They found that nonnative species are slowly, but steadily, increasing in all three parameters in the Yaqui Basin (Unmack and Fagan 2004, p. 233). Unmack and Fagan (2004, p. 233) predicted that, in the absence of aggressive management intervention, significant extirpations or range reductions of native fish species are expected to occur in the Yaqui Basin of Sonora, Mexico, which may have extant populations of the northern Mexican gartersnake, as did much of the Gila Basin before the introduction of nonnative species. Loss of native fishes will impact prey availability for the northern Mexican gartersnake and threaten its persistence in these areas. Black bullheads (

Ameiurus melas

) were reported as abundant, and common carp were detected from the Rio Yaqui in southern Sonora, Mexico (Branson

et al.

1960, p. 219). Bluegill (

Lepomis macrochirus

) were also reported at this location, representing a significant range expansion that the authors expected was the result of escaping nearby farm ponds or irrigation ditches (Branson

et al.

1960, p. 220). Largemouth bass, green sunfish, and an undetermined crappie species have also been reported from this area (Branson

et al.

1960, p. 220). Hendrickson and Varela-Romero (1989, p. 479) conducted fish sampling along the Río Sonoyta of northern Sonora, Mexico, and found over half of the fish collected were nonnative, both predatory species and prey species for the northern Mexican gartersnake.

Domínguez-Domínguez

et al.

(2007, p. 171) sampled 52 localities for a rare freshwater fish, the Picotee goodeid (

Zoogoneticus quitzeoensis

), along the southern portion of the Mesa Central (Mexican Plateau) of Mexico and found 21 localities had significant signs of pollution. Of the 29 localities where the target species was detected, 28 of them also had harmful nonnative species

present, such as largemouth bass, cichlids (

Oreochromis

sp.), bluegill, Pátzcuaro chub (

Algansea lacustris

) (Domínguez-Domínguez

et al.

2007, pp. 171, Table 3). Other nonnative fish species reported are soft-rayed and small bodied, and may be prey items for younger age classes of northern Mexican gartersnakes. Several examples of significant aquatic habitat degradation or destruction were also observed by Domínguez-Domínguez

et al.

(2007, Table 3) in this region of Mexico, including the draining of natural lakes and cienegas for conversion to agricultural purposes, modification of springs for recreational swimming, diversions, and dam construction. As of 2006, native fish species comprised the most prevalent in species composition and abundance in the Laja Basin; however the basin is trending towards a nonnative fishery based on historical data whereas nonnative species were most recently collected from 16 of 17 sample sites, largemouth bass have significantly expanded their distribution within the headwaters of the basin, and bluegill are now widespread in the Laja River (Mercado-Silva

et al.

2006, pp. 537, 542, Table 4).

The ecological risk of nonnative, freshwater aquaculture production has only recently been acknowledged by the Mexican government as compared to decades of aquaculture production, mainly because conservation of biodiversity was not valued as highly as the benefits garnered by nonnative fish production, most notably in the country's rural, poorest regions (Tapia and Zambrano 2003, p. 252). In fact, recent amendments to Mexico's fishing regulations allow for relaxation of existing regulations imposed by other government regulations and expansion of opportunities for investment in commercial fishing to promote growth in Mexico's aquaculture sector (Sugunan 1997, Section 8.7.1). Between the broad geographic extent of commercial or sustenance fisheries, the important source of protein they represent, and the many mechanisms introduced nonnative fish have to naturally or artificially expand their distribution, few areas within the range of the northern Mexican gartersnake in Mexico have avoided adverse impacts associated with nonnative species. Harmful nonnative fish species therefore pose a significant threat to the prey base of northern Mexican gartersnakes and to the gartersnakes themselves throughout most of their range in Mexico.

Amphibian decline

—Matthews

et al.

(2002, p. 16) examined the relationship of gartersnake distributions, amphibian population declines, and nonnative fish introductions in high-elevation aquatic ecosystems in California. Matthews

et al.

(2002, p. 16) specifically examined the effect of nonnative trout introductions on populations of amphibians and mountain gartersnakes (

Thamnophis elegans elegans

). Their results indicated the probability of observing gartersnakes was 30 times greater in lakes containing amphibians than in lakes where amphibians have been extirpated by nonnative fish. These results supported a prediction by Jennings

et al.

(1992, p. 503) that native amphibian declines will lead directly to gartersnake declines. Matthews

et al.

(2002, p. 20) noted that, in addition to nonnative fish species adversely impacting amphibian populations that are part of the gartersnake's prey base, direct predation on gartersnakes by nonnative fish also occurs. However, Shah

et al.

(2010, pp. 188-190) found that native tadpoles may exhibit anti-predator learning behavior that may assist their persistence in habitat affected by nonnative, spiny-rayed fish.

Declines in the native leopard frog populations in Arizona have contributed to declines in the northern Mexican gartersnake, one of the frog's primary native predators. Native ranid frog species, such as lowland leopard frogs, northern leopard frogs, and federally threatened Chiricahua leopard frogs, have all experienced declines in various degrees throughout their distribution in the Southwest, partially due to predation and competition with nonnative species (Clarkson and Rorabaugh 1989, pp. 531, 535; Hayes and Jennings 1986, p. 490). Rosen

et al.

(1995, pp. 257-258) found that Chiricahua leopard frog distribution in the Chiricahua Mountain region of Arizona was inversely related to nonnative species distribution and, without corrective action, predicted that the Chiricahua leopard frog may be difficult to conserve in this region. Along the Mogollon Rim, Holycross

et al.

(2006, p. 13) found that only 8 sites of 57 surveyed (15 percent) consisted of an entirely native anuran community, and that native frog populations in another 19 sites (33 percent) had been completely displaced by invading bullfrogs. However, such declines in native frog populations are not necessarily irreversible. Ranid frog populations have been shown to rebound strongly when nonnative fish are removed (Knapp

et al.

2007, pp. 15-18).

Scotia Canyon, in the Huachuca Mountains of southeastern Arizona, is a location where corresponding declines of leopard frog and northern Mexican gartersnake populations have been documented through repeated survey efforts over time (Holm and Lowe 1995, p. 33). Surveys of Scotia Canyon occurred during the early 1980s, and again during the early 1990s. Leopard frogs in Scotia Canyon were infrequently observed during the early 1980s, and were apparently extirpated by the early 1990s (Holm and Lowe 1995, pp. 45-46). Northern Mexican gartersnakes were observed in decline during the early 1980s, with low capture rates continuing through the early 1990s (Holm and Lowe 1995, pp. 27-35). Surveys documented further decline of leopard frogs and northern Mexican gartersnakes in 2000 (Rosen

et al.

2001, pp. 15-16).

A former large, local population of northern Mexican gartersnakes at the San Bernardino National Wildlife Refuge (SBNWR) in southeastern Arizona has also experienced a correlative decline of leopard frogs, and northern Mexican gartersnakes are now thought to occur at very low-population densities or may be extirpated there (Rosen and Schwalbe 1988, p. 28; 1995, p. 452; 1996, pp. 1-3; 1997, p. 1; 2002b, pp. 223-227; 2002c, pp. 31, 70; Rosen

et al.

1996b, pp. 8-9; 2001, pp. 6-10).

Survey data indicate that declines of leopard frog populations, often correlated with nonnative species introductions, the spread of a chytrid fungus (

Batrachochytrium dendrobatidis,

Bd), and habitat modification and destruction, have occurred throughout much of the northern Mexican gartersnake's U.S. distribution (Nickerson and Mays 1970, p. 495; Vitt and Ohmart 1978, p. 44; Ohmart

et al.

1988, p. 150; Rosen and Schwalbe 1988, Appendix I; 1995, p. 452; 1996, pp. 1-3; 1997, p. 1; 2002b, pp. 232-238; 2002c, pp. 1, 31; Clarkson and Rorabaugh 1989, pp. 531-538; Sredl

et al.

1995a, pp. 7-8; 1995b, pp. 8-9, 1995c, pp. 7-8; 2000, p. 10; Holm and Lowe 1995, pp. 45-46; Rosen

et al.

1996b, p. 2; 2001, pp. 2, 22; Degenhardt

et al.

1996, p. 319; Fernandez and Rosen 1996, pp. 6-20; Drost and Nowak 1997, p. 11; Turner

et al.

1999, p. 11; Nowak and Spille 2001, p. 32; Holycross

et al.

2006, pp. 13-14, 52-61). Specifically, Holycross

et al.

(2006, pp. 53-57, 59) documented potential extirpations of the northern Mexican gartersnake's native leopard frog prey base at several currently, historically, or potentially occupied locations, including the Agua Fria River in the vicinity of Table Mesa Road and Little Grand Canyon Ranch, and at Rock Springs, Dry Creek from Dugas Road to Little Ash Creek, Little Ash Creek from Brown Spring to Dry Creek, Sycamore Creek (Agua Fria

subbasin) in the vicinity of the Forest Service Cabin, the Page Springs and Bubbling Ponds fish hatchery along Oak Creek, Sycamore Creek (Verde River subbasin) in the vicinity of the confluence with the Verde River north of Clarkdale, along several reaches of the Verde River mainstem, Cherry Creek on the east side of the Sierra Ancha Mountains, and Tonto Creek from Gisela to “the Box,” near its confluence with Rye Creek.

Rosen

et al.

(2001, p. 22) identified the expansion of bullfrogs into the Sonoita grasslands, which contain occupied northern Mexican gartersnake habitat, and the introduction of crayfish into Lewis Springs, as being of particular concern in terms of future recovery efforts for the northern Mexican gartersnake. Rosen

et al.

(1995, pp. 252-253) sampled aquatic herpetofauna at 103 sites in the Chiricahua Mountains region, which included the Chiricahua, Dragoon, and Peloncillo mountains, and the Sulphur Springs, San Bernardino, and San Simon valleys. They found that 43 percent of all cold-blooded aquatic and semi-aquatic vertebrate species detected were nonnative. The most commonly encountered nonnative species was the bullfrog (Rosen

et al.

1995, p. 254). Witte

et al.

(2008, p. 1) found that the disappearance of ranid frog populations in Arizona were 2.6 times more likely in the presence of crayfish. Witte

et al.

(2008, p. 7) emphasized the significant influence of nonnative species on the disappearance of ranid frogs in Arizona.

In addition to harmful nonnative species, disease and nonnative parasites have been implicated in the decline of the prey base of the northern Mexican gartersnake. In particular, the outbreak of chytridiomycosis or “Bd,” a skin fungus, has been identified as a chief causative agent in the significant declines of many of the native ranid frogs and other amphibian species. In addition, regional concerns exist for the native fish community due to nonnative parasites, such as the Asian tapeworm (

Bothriocephalus acheilognathi

) in southeastern Arizona (Rosen and Schwalbe 1997, pp. 14-15; 2002c, pp. 1-19; Morell 1999, pp. 728-732; Sredl and Caldwell 2000, p. 1; Hale 2001, pp. 32-37; Bradley

et al.

2002, p. 206). As indicated, Bd has been implicated in both large-scale declines and local extirpations of many amphibians, chiefly anuran species, around the world (Johnson 2006, p. 3011). Lips

et al.

(2006, pp. 3166-3169) suggest that the high virulence and large number of potential hosts make Bd a serious threat to amphibian diversity. In Arizona, Bd infections have been reported in several of the native prey species of the northern Mexican gartersnake within the distribution of the snake (Morell 1999, pp. 731-732; Sredl and Caldwell 2000, p. 1; Hale 2001, pp. 32-37; Bradley

et al.

2002, p. 207; USFWS 2002, pp. 40802-40804; USFWS 2007, pp. 26, 29-32). Declines of native prey species of the northern Mexican gartersnake from Bd infections have contributed to the decline of this species in the United States (Morell 1999, pp. 731-732; Sredl and Caldwell 2000, p. 1; Hale 2001, pp. 32-37; Bradley

et al.

2002, p. 207; USFWS 2002, pp. 40802-40804; USFWS 2007, pp. 26, 29-32). Evidence of Bd-related amphibian declines has been confirmed in portions of southern Mexico (just outside the range of northern Mexican gartersnakes), and data suggest declines are more prevalent at higher elevations (Lips

et al.

2004, pp. 560-562). However, much less is known about the role of Bd in amphibian declines across much of Mexico, in particular the mountainous regions of Mexico (including much of the range of northern Mexican gartersnakes in Mexico) as the region is significantly understudied (Young

et al.

2000, p. 1218). Because narrow-headed gartersnakes feed on fish, Bd has not affected their prey base. Also, research shows that the fungus

Batrachochytrium

can grow on boiled snakeskin (keratin) in the laboratory (Longcore

et al.

1999, p. 227), indicating the potential for disease outbreaks in wild snake populations if conditions are favorable; however no observations have been made in the field, and we found no other data that propose a direct linkage between Bd and snake mortality.

The Effects of Bullfrogs on Native Aquatic Communities

Bullfrogs are generally considered one of the most serious threats to northern Mexican gartersnakes throughout their range (Conant 1974, pp. 471, 487-489; Rosen and Schwalbe 1988, pp. 28-30; Rosen

et al.

2001, pp. 21-22). Bullfrogs have and do threaten some populations of narrow-headed gartersnakes, but differing habitat preferences between the two temper their effect on narrow-headed gartersnakes. Bullfrogs adversely affect northern Mexican and narrow-headed gartersnakes through direct predation of juveniles and sub-adults. Bullfrogs also compete with northern Mexican gartersnakes. Bullfrogs are not native to the southwestern United States or Mexico, and first appeared in Arizona in 1926, as a result of a systematic introduction effort by the State Game Department (now, the AGFD) for the purposes of sport hunting and as a food source (Tellman 2002, p. 43). We are not certain when bullfrogs were first reported from New Mexico but presume it was many decades ago. Bullfrogs are extremely prolific, are strong colonizers, and may disperse distances of up to 10 mi (16 km) across uplands, and likely further within drainages (Bautista 2002, p. 131; Rosen and Schwalbe 2002a, p. 7; Casper and Hendricks 2005, p. 582; Suhre 2008, pers. comm.).

Bullfrogs are large-bodied, voracious, opportunistic, even cannibalistic predators that readily attempt to consume any living thing smaller than them. Bullfrogs have a highly varied diet, which has been documented to include vegetation, invertebrates, fish, birds, mammals, amphibians, and reptiles, including numerous species of snakes (eight genera, including six different species of gartersnakes, two species of rattlesnakes, and Sonoran gophersnakes (

Pituophis catenifer affinis

)) (Bury and Whelan 1984, p. 5; Clarkson and DeVos 1986, p. 45; Holm and Lowe 1995, pp. 37-38; Carpenter

et al.

2002, p. 130; King

et al.

2002; Hovey and Bergen 2003, pp. 360-361; Casper and Hendricks 2005, pp. 543-544; Combs

et al.

2005, p. 439; Wilcox 2005, p. 306; DaSilva

et al.

2007, p. 443; Neils and Bugbee 2007, p. 443; Rowe and Garcia 2012, pp. 633-634). In one study, three different species of gartersnakes (

Thamnophis sirtalis, T. elegans,

and

T. ordinoides

) totaling 11 snakes were found inside the stomachs of resident bullfrogs from a single region (Jancowski and Orchard 2013, p. 26). Bullfrogs can significantly reduce or eliminate the native amphibian populations (Moyle 1973, pp. 18-22; Conant 1974, pp. 471, 487-489; Hayes and Jennings 1986, pp. 491-492; Rosen and Schwalbe 1988, pp. 28-30; 2002b, pp. 232-238; Rosen

et al.

1995, pp. 257-258; 2001, pp. 2, Appendix I; Wu

et al.

2005, p. 668; Pearl

et al.

2004, p. 18; Kupferberg 1994, p. 95; Kupferburg 1997, pp. 1736-1751; Lawler

et al.

1999; Bury and Whelan 1986, pp. 9-10; Hayes and Jennings 1986, pp. 500-501; Jones and Timmons 2010, pp. 473-474), which are vital for northern Mexican gartersnakes. Different age classes of bullfrogs within a community can affect native ranid populations via different mechanisms. Juvenile bullfrogs affect native ranids through competition, male bullfrogs affect native ranids through predation, and female bullfrogs affect native ranids through both mechanisms depending on body size and microhabitat (Wu

et al.

2005, p. 668). Pearl

et al.

(2004, p. 18) also suggested that the effect of bullfrog introductions on native ranids may be different based

on specific habitat conditions, but also suggested that an individual ranid frog species' physical ability to escape influences the effect of bullfrogs on each native ranid community.

Bullfrogs have been documented throughout the State of Arizona. Holycross

et al.

(2006, pp. 13-14, 52-61) found bullfrogs at 55 percent of sample sites in the Agua Fria subbasin, 62 percent of sites in the Verde River subbasin, 25 percent of sites in the Salt River subbasin, and 22 percent of sites in the Gila River subbasin. In total, bullfrogs were observed at 22 of the 57 sites surveyed (39 percent) across the Mogollon Rim (Holycross

et al.

2006, p. 13). A number of authors have also documented the presence of bullfrogs through their survey efforts throughout many subbasins in Arizona and New Mexico adjacent to the historical distribution of the northern Mexican or narrow-headed gartersnake, including northern Arizona (Sredl

et al.

1995a, p. 7; 1995c, p. 7), central Arizona and along the Mogollon Rim of Arizona and New Mexico (Nickerson and Mays 1970, p. 495; Hulse 1973, p. 278; Sredl

et al.

1995b, p. 9; Drost and Nowak 1997, p. 11; Nowak and Spille 2001, p. 11; Holycross

et al.

2006, pp. 15-51; Wallace

et al.

2008; pp. 243-244; Helleckson 2012a, pers. comm.), southern Arizona (Rosen and Schwalbe 1988, Appendix I; 1995, p. 452; 1996, pp. 1-3; 1997, p. 1; 2002b, pp. 223-227; 2002c, pp. 31, 70; Holm and Lowe 1995, pp. 27-35; Rosen

et al.

1995, p. 254; 1996a, pp. 16-17; 1996b, pp. 8-9; 2001, Appendix I; Turner

et al.

1999, p. 11; Sredl

et al.

2000, p. 10; Turner 2007; p. 41), and along the Colorado River (Vitt and Ohmart 1978, p. 44; Clarkson and DeVos 1986, pp. 42-49; Ohmart

et al.

1988, p. 143). In one of the more conspicuous examples, bullfrogs were identified as the primary cause for collapse of both the northern Mexican gartersnake and its prey base on the SBNWR (Rosen and Schwalbe 1988, p. 28; 1995, p. 452; 1996, pp. 1-3; 1997, p. 1; 2002b, pp. 223-227; 2002c, pp. 31, 70; Rosen

et al.

1996b, pp. 8-9).

Perhaps one of the most serious consequences of bullfrog introductions is their persistence in an area once they have become established, and the subsequent difficulty in eliminating bullfrog populations. Rosen and Schwalbe (1995, p. 452) experimented with bullfrog removal at various sites on the SBNWR, in addition to a control site with no bullfrog removal in similar habitat on the Buenos Aires National Wildlife Refuge (BANWR). Removal of adult bullfrogs, without removal of eggs and tadpoles, resulted in a substantial increase in younger age-class bullfrogs where removal efforts were the most intensive (Rosen and Schwalbe 1997, p. 6). Contradictory to the goals of bullfrog eradication, evidence from dissection samples from young adult and sub-adult bullfrogs indicated these age-classes readily prey upon juvenile bullfrogs (up to the average adult leopard frog size) as well as juvenile gartersnakes, which suggests that the selective removal of only the large adult bullfrogs (presumed to be the most dangerous size class to leopard frogs and gartersnakes), favoring the young adult and sub-adult age classes, could indirectly lead to increased predation of leopard frogs and juvenile gartersnakes (Rosen and Schwalbe 1997, p. 6). These findings illustrate that in addition to large adults, subadult bullfrogs also negatively impact northern Mexican gartersnakes and their prey species. It also indicates the importance of including egg mass and tadpole removal during efforts to control bullfrogs and timing removal projects to ensure reproductive bullfrogs are removed prior to breeding. Some success in regional bullfrog eradication has been had in a few cases described below in the section entitled “

Current Conservation of Northern Mexican and Narrow-headed Gartersnakes.

”

Bullfrogs not only compete with the northern Mexican gartersnake for prey items but directly prey upon juvenile and occasionally sub-adult northern Mexican and narrow-headed gartersnakes (Rosen and Schwalbe 1988, pp. 28-31; 1995, p. 452; 2002b, pp. 223-227; Holm and Lowe 1995, pp. 29-29; Rossman

et al.

1996, p. 177; AGFD

In Prep.,

p. 12; 2001, p. 3; Rosen

et al.

2001, pp. 10, 21-22; Carpenter

et al.

2002, p. 130; Wallace 2002, p. 116). A well-circulated photograph of an adult bullfrog in the process of consuming a northern Mexican gartersnake at Parker Canyon Lake, Cochise County, Arizona, taken by John Carr of the Arizona Game and Fish Department in 1964, provides photographic documentation of bullfrog predation (Rosen and Schwalbe 1988, p. 29; 1995, p. 452). The most recent, physical evidence of bullfrog predation of northern Mexican gartersnakes is provided in photographs of a dissected bullfrog at Pasture 9 Tank in the San Rafael Valley of Arizona that had a freshly-eaten neonatal northern Mexican gartersnake in its stomach (Akins 2012, pers. comm.).

A common observation in northern Mexican gartersnake populations that co-occur with bullfrogs is a preponderance of large, mature adult snakes with conspicuously low numbers of individuals in the newborn and juvenile age size classes due to bullfrogs more effectively preying on young small snakes, which ultimately leads to low reproductive rates and survival of young (Rosen and Schwalbe 1988, p. 18; Holm and Lowe 1995, p. 34). In lotic (flowing water) systems, bullfrogs prefer sites with low or limited flow, such as backwaters, side channels, and pool habitat. These areas are also used frequently by northern Mexican and narrow-headed gartersnakes, which likely results in increased predation rates and likely depressed recruitment of gartersnakes. Potential recruitment problems for northern Mexican gartersnakes due to effects from nonnative species are suspected at Tonto Creek (Wallace

et al.

2008, pp. 243-244). Rosen and Schwalbe (1988, p. 18) stated that the low recruitment at the SBNWR, a typical characteristic of gartersnake populations affected by harmful nonnative species, is the likely cause of that populations' decline and possibly for declines in populations throughout their range in Arizona. Specific localities within the distribution of northern Mexican and narrow-headed gartersnakes where bullfrogs have been detected are presented in Appendix A (available at

http://www.regulations.gov

under Docket No. FWS-R2-ES-2013-0071).

The Effects of Crayfish on Native Aquatic Communities

Crayfish are a nonnative species in Arizona and New Mexico and are a primary threat to many prey species of northern Mexican and narrow-headed gartersnakes, and may also prey upon juvenile gartersnakes themselves (Fernandez and Rosen 1996, p. 25; Voeltz 2002, pp. 87-88; USFWS 2007, p. 22). Fernandez and Rosen (1996, p. 3) studied the effects of crayfish introductions on two stream communities in Arizona, a low-elevation semi-desert stream and a high mountain stream, and concluded that crayfish can noticeably reduce species diversity and destabilize food chains in riparian and aquatic ecosystems through their effect on vegetative structure, stream substrate (stream bottom;

i.e.,

silt, sand, cobble, boulder) composition, and predation on eggs, larval, and adult forms of native invertebrate and vertebrate species. Crayfish fed on embryos, tadpoles, newly metamorphosed frogs, and adult leopard frogs, but they did not feed on egg masses (Fernandez and Rosen 1996, p. 25). However, Gamradt and Kats (1996, p. 1155) found that crayfish readily consumed the egg masses of California newts (

Taricha torosa

). Crayfish are known to also eat fish eggs and larva (Inman

et al.

1998, p. 17), especially those bound to the substrate (Dorn and

Mittlebach 2004, p. 2135). Fernandez and Rosen (1996, pp. 6-19, 52-56) and Rosen (1987, p. 5) discussed observations of inverse relationships between crayfish abundance and native reptile and amphibian populations, including narrow-headed gartersnakes, northern leopard frogs, and Chiricahua leopard frogs. Crayfish may also affect native fish populations. Carpenter (2005, pp. 338-340) documented that crayfish may reduce the growth rates of native fish through competition for food and noted that the significance of this impact may vary between species.

Crayfish alter the abundance and structure of aquatic vegetation by grazing on aquatic and semiaquatic vegetation, which reduces the cover needed by frogs and gartersnakes, as well as the food supply for prey species such as tadpoles (Fernandez and Rosen 1996, pp. 10-12). Fernandez and Rosen (1996, pp. 10-12) found that crayfish frequently burrow into stream banks, leading to increased bank erosion, stream turbidity, and siltation of stream bottoms. Creed (1994, p. 2098) found that filamentous alga (

Cladophora glomerata

) was at least 10-fold greater in aquatic habitats that lacked crayfish. Filamentous alga is an important component of aquatic vegetation that provides cover for foraging gartersnakes, as well as microhabitat for prey species.

Crayfish have recently been found to also act as a host for the amphibian disease-causing fungus, Bd (McMahon

et al.

(2013, pp. 210-213). This could have serious implications for northern Mexican gartersnakes because crayfish can now be considered a source of disease in habitat that is devoid of amphibians but otherwise potentially suitable habitat for immigrating amphibians, such as leopard frogs, which could serve as a prey base. Because crayfish are so widespread throughout Arizona, New Mexico, and portions of Mexico, this could have broad, negative implications for the recovery of native leopard frogs, and therefore the recovery of northern Mexican gartersnakes.

Inman

et al.

(1998, p. 3) documented crayfish as widely distributed and locally abundant in a broad array of natural and artificial free-flowing and still-water habitats throughout Arizona, many of which overlap the historical and current distribution of northern Mexican and narrow-headed gartersnakes. Hyatt (undated, p. 71) concluded that the majority of waters in Arizona contained at least one species of crayfish. In surveying for northern Mexican and narrow-headed gartersnakes, Holycross

et al.

(2006, p. 14) found crayfish in 64 percent of the sample sites in the Agua Fria subbasin; in 85 percent of the sites in the Verde River subbasin; in 46 percent of the sites in the Salt River subbasin; and in 67 percent of the sites in the Gila River subbasin. In total, crayfish were observed at 35 (61 percent) of the 57 sites surveyed across the Mogollon Rim (Holycross

et al.

2006, p. 14), most of which were sites historically or currently occupied by northern Mexican or narrow-headed gartersnakes, or sites the investigators believed possessed suitable habitat and may be occupied by these gartersnakes based upon the their known historical distributions.

A number of authors have documented the presence of crayfish through their survey efforts throughout Arizona and New Mexico in specific regional areas, drainages, and lentic wetlands within or adjacent to the historical distribution of the northern Mexican or narrow-headed gartersnake, including northern Arizona (Sredl

et al.

1995a, p. 7; 1995c, p. 7), central Arizona and along the Mogollon Rim of Arizona and New Mexico (Sredl

et al.

1995b, p. 9; Fernandez and Rosen 1996, pp. 54-55, 71; Inman

et al.

1998, Appendix B; Nowak and Spille 2001, p. 33; Holycross

et al.

2006, pp. 15-51; Brennan 2007, p. 7; Burger 2008, p. 4; Wallace

et al.

2008; pp. 243-244; Brennan and Rosen 2009, p. 9; Karam

et al.

2009; pp. 2-3; Helleckson 2012a, pers. comm.), southern Arizona (Rosen and Schwalbe 1988, Appendix I; Inman

et al.

1998, Appendix B; Sredl

et al.

2000, p. 10; Rosen

et al.

2001, Appendix I), and along the Colorado River (Ohmart

et al.

1988, p. 150; Inman

et al.

1998, Appendix B). Specific localities within the distribution of northern Mexican and narrow-headed gartersnakes where crayfish have been detected are presented in Appendix A (available at

http://www.regulations.gov

under Docket No. FWS-R2-ES-2013-0071).

Like bullfrogs, crayfish can be very difficult, if not impossible, to eradicate once they have become established in an area, depending on the complexity of the habitat (Rosen and Schwalbe 1996a, pp. 5-8; 2002a, p. 7; Hyatt undated, pp. 63-71). The use of biological control agents such as bacteria, nematodes, and viruses were explored in addressing the invasion and persistence of crayfish in the southwestern United States, using the organisms' cannibalistic nature as a vector (Davidson

et al.

2010, pp. 297-310). The use of biological control agents tested found them to be ineffective or infeasible in controlling crayfish, but a number of other biological pathogens have been described in freshwater crayfish that may lend promise to finding an appropriate control agent in the future (Davidson

et al.

2010, pp. 307-308). In addition, recent experimentation with ammonia as a piscicide indirectly found that crayfish were also effectively eradicated in field trials; the first successful and most promising control method for this harmful nonnative species in recent times (Ward

et al.

2013, pp. 402-404). However, it could be potentially several years before ammonia is licensed for such use, if ever.

The Effects of Predation-Related Injuries to Gartersnakes

The tails of gartersnakes are often broken off during predation attempts by bullfrogs or crayfish and do not regenerate. The incidence of tail breaks in gartersnakes can often be used to assess predation pressure within gartersnake populations. Attempted predation occurs on both sexes and all ages of gartersnakes within a population, although some general trends have been detected. For example, female gartersnakes may be more susceptible to predation as evidenced by the incidence of tail damage (Willis

et al.

1982, pp. 100-101; Rosen and Schwalbe1988, p. 22; Mushinsky and Miller 1993, pp. 662-664; Fitch 2003, p. 212). This can be explained by higher basking rates associated with pregnant females that increase their visibility to predators. Fitch (2003, p. 212) found that tail injuries in the common gartersnake occurred more frequently in adults than in juveniles. Predation on juvenile snakes likely results in complete consumption of the animal, which would limit observations of tail injury in their age class.

Tail injuries can have negative effects on the health, longevity, and overall success of individual gartersnakes from infection, slower swimming and crawling speeds, or impeding reproduction. Mushinsky and Miller (1993, pp. 662-664) commented that, while tail breakage in gartersnakes can save the life of an individual snake, it also leads to permanent handicapping of the snake, resulting in slower swimming and crawling speeds, which could leave the snake more vulnerable to predation or affect its foraging ability. Willis

et al.

(1982, p. 98) discussed the incidence of tail injury in three species in the genus

Thamnophis

(common gartersnake, Butler's gartersnake (

T. butleri

), and the eastern ribbon snake (

T. sauritus

)) and concluded that individuals that suffered nonfatal injuries prior to reaching a length of 12 in (30 cm) are not likely to survive and that physiological stress during post-injury hibernation may play an important role in subsequent

mortality. While northern Mexican or narrow-headed gartersnakes may survive an individual predation attempt from a bullfrog or crayfish with tail damage, secondary effects from infection of the wound may significantly contribute to mortality of individuals. Perry-Richardson

et al.

(1990, p. 77) described the importance of tail-tip alignment in the successful courtship and mating in Thamnophiine snakes and found that missing or shortened tails adversely affected these activities and, therefore, mating success. In researching the role of tail length in mating success in the red-sided gartersnake (

Thamnophis sirtalis parietalis

), Shine

et al.

(1999, p. 2150) found that males that experienced injuries or the partial or whole loss of the tail experienced a three-fold decrease in mating success.

The frequency of tail injuries can be quite high in a given gartersnake population; for example at the SBNWR (Rosen and Schwalbe 1988, pp. 28-31), 78 percent of northern Mexican gartersnakes had broken tails with a “soft and club-like” terminus, which suggests repeated injury from multiple predation attempts by bullfrogs. While medically examining pregnant female northern Mexican gartersnakes, Rosen and Schwalbe (1988, p. 28) noted bleeding from the posterior region, which suggested to the investigators the snakes suffered from “squeeze-type” injuries inflicted by adult bullfrogs. In another example, Holm and Lowe (1995, pp. 33-34) observed tail injuries in 89 percent of northern Mexican gartersnakes during the early 1990s in Scotia Canyon in the Huachuca Mountains, as well as a skewed age class ration that favored adults over subadults, which is consistent with data collected by Willis

et al.

(1982, pp. 100-101) on other gartersnake species. Bullfrogs are largely thought to be responsible for the significant decline of northern Mexican gartersnake and its prey base at this locality, although the latter has improved through recovery actions. In the Black River, crayfish are very abundant and have been identified as the likely cause for a high-frequency of tail injuries to narrow-headed gartersnakes (Brennan 2007, p. 7; Brennan and Rosen 2009, p. 9). Brennan (2007, p. 5) found that in the Black River, 14 of 15 narrow-headed gartersnakes captured showed evidence of damaged or missing tails (Brennan 2007, p. 5). In 2009, 16 of 19 narrow-headed gartersnakes captured in the Black River showed evidence of damaged or missing tails (Brennan and Rosen 2009, p. 8). In the upper Verde River region, Emmons and Nowak (2013, p. 5) reported that 18 of 49 (37 percent) northern Mexican gartersnakes captured had scars (n = 17) and/or missing tails tips (n = 7).

Vegetation or other forms of protective cover may be particularly important for gartersnakes to reduce the effects of harmful nonnative species on populations. For example, the population of northern Mexican gartersnakes at the Page Springs and Bubbling Ponds State Fish Hatcheries occurs with harmful nonnative species (Boyarski 2008b, pp. 3-4, 8). Yet, only 11 percent of northern Mexican gartersnakes captured in 2007 were observed as having some level of tail damage (Boyarski 2008b, pp. 5, 8). The relatively low occurrence of tail damage, as compared to 78 percent of snakes with tail damage found by Rosen and Schwalbe (1988, pp. 28-31), may indicate: (1) Adequate vegetation density was used by gartersnakes to avoid harmful nonnative species predation attempts; (2) a relatively small population of harmful nonnative species may be at a comparatively lower density than sites sampled by previous studies (harmful nonnative species population density data were not collected by Boyarski (2008b)); (3) gartersnakes may not have needed to move significant distances at this locality to achieve foraging success, which might reduce the potential for encounters with harmful nonnative species; or (4) gartersnakes infrequently escaped predation attempts by harmful nonnative species, were removed from the population, and were consequently not detected by surveys.

The Expansion of the American Bullfrog and Crayfish in Mexico

Bullfrogs have recently been documented as a significant threat to native aquatic and riparian species throughout Mexico. Luja and Rodríguez-Estrella (2008, pp. 17-22) examined the invasion of the bullfrog in Mexico. The earliest records of bullfrogs in Mexico were Nuevo Leon (1853), Tamaulipas (1898), Morelos (1968), and Sinaloa (1969) (Luja and Rodríguez-Estrella 2008, p. 20). By 1976, the bullfrog was documented in seven more states: Aguacalientes, Baja California Sur, Chihuahua, Distrito Federal, Puebla, San Luis Potosi, and Sonora (Luja and Rodríguez-Estrella 2008, p. 20). The bullfrog was recently verified from the state of Hidalgo, Mexico, at an elevation of 8,970 feet (2,734 m), which indicates the species continues to spread in that country and can exist even at the uppermost elevations inhabited by northern Mexican gartersnakes (Duifhuis Rivera

et al.

2008, p. 479). As of 2008, Luja and Rodríguez-Estrella (2008, p. 20) have recorded bullfrogs in 20 of the 31 Mexican States (65 percent of the states in Mexico) and suspect that they have invaded other States, but were unable to find documentation.

Sponsored by the then Mexican Secretary of Aquaculture Support, bullfrogs have been commercially produced for food in Mexico in Yucatan, Nayarit, Morelos, Estado de Mexico, Michoacán, Guadalajara, San Luis Potosi, Tamaulipas, and Sonora (Luja and Rodríguez-Estrella 2008, p. 20). However, frog legs ultimately never gained popularity in Mexican culinary culture (Conant 1974, pp. 487-489), and Luja and Rodríguez-Estrella (2008, p. 22) point out that only 10 percent of these farms remain in production. Luja and Rodríguez-Estrella (2008, pp. 20, 22) document instances where bullfrogs have escaped production farms and suspect the majority of the frogs that were produced commercially in farms that have since ceased operation have assimilated into surrounding habitat.

Luja and Rodríguez-Estrella (2008, p. 20) also state that Mexican people deliberately introduce bullfrogs for ornamental purposes, or “for the simple pleasure of having them in ponds.” The act of deliberately releasing bullfrogs into the wild in Mexico was cited by Luja and Rodríguez-Estrella (2008, p. 21) as being “more common than we can imagine.” Bullfrogs are available for purchase at some Mexican pet stores (Luja and Rodríguez-Estrella 2008, p. 22). Luja and Rodríguez-Estrella (2008, p. 21) state that bullfrog eradication efforts in Mexico are often thwarted by their popularity in rural communities (presumably as a food source). Currently, no regulation exists in Mexico to address the threat of bullfrog invasions or prevent their release into the wild (Luja and Rodríguez-Estrella 2008, p. 22).

Rosen and Melendez (2006, p. 54) report bullfrog invasions to be prevalent in northwestern Chihuahua and northwestern Sonora, where the northern Mexican gartersnake is thought to occur. In many areas, native leopard frogs were completely displaced where bullfrogs were observed. Rosen and Melendez (2006, p. 54) also demonstrated the relationship between fish and amphibian communities in Sonora and western Chihuahua. Native leopard frogs, a primary prey item for the northern Mexican gartersnake, only occurred in the absence of nonnative fish, and were absent from waters containing nonnative species, which included several major waters. In Sonora, Rorabaugh (2008a, p. 25) also

considers the bullfrog to be a significant threat to the northern Mexican gartersnake and its prey base, substantiated by field observations made during surveys conducted in Chihuahua and Sonora in 2006 (Rorabaugh 2008b, p. 1).

Few data were found on the presence or distribution of nonnative crayfish species in Mexico. However, in a 2-week gartersnake survey effort in 2006 in northern Mexico, crayfish were observed as “widely distributed” in the valleys of western Chihuahua (Rorabaugh 2008b, p. 1). Based on the invasive nature of crayfish ecology and their distribution in the United States along the Border region, it is reasonable to assume that, at a minimum, crayfish are likely distributed along the entire Border region of northern Mexico, adjacent to where they occur in the United States.

Risks to Gartersnakes From Fisheries Management Activities

The decline in native fish communities from the effects of harmful nonnative fish species has spurred resource managers to take action to help recover native fish species. While we fully support activities designed to help recover native fish, recovery actions for native fish, in the absence of thorough planning, can have significant adverse effects on resident gartersnake populations.

Piscicides

—Piscicide is a term that refers to a “fish poison.” The use of piscicides, such as rotenone or antimycin A, for the removal of harmful nonnative fish species has widely been considered invaluable for the conservation and recovery of imperiled native fish species throughout the United States, and in particular the Gila River basin of Arizona and New Mexico (Dawson and Kolar 2003, entire). Antimycin A is rarely used anymore, and has been largely replaced by rotenone in field applications. Experimentation with ammonia as a piscicide has shown promising results and may ultimately replace rotenone in the future as a desired control method if legally registered for such use (Ward

et al.

2013, pp. 402-404). Currently, rotenone is the most commonly used piscicide. The active ingredient in rotenone is a natural chemical compound extracted from the stems and roots of tropical plants in the family Leguminosae that interrupts oxygen absorption in gill-breathing animals (Fontenot

et al.

1994, pp. 150-151). In the greater Gila River subbasin alone, 57 streams or water bodies have been treated with piscicide, some on several occasions spanning many years (Carpenter and Terrell 2005; Table 6). However, this practice has been the source of recent controversy due to a perceived link between rotenone and Parkinson's disease in humans, as well as potential effects to livestock. Speculation of the potential role of rotenone in Parkinson's disease was fueled by Tanner

et al.

(2011, entire) which correlated the incidence of the disease with lifetime exposure to certain pesticides, including rotenone. As a result, in 2012, the Arizona State Legislature proposed two bills that called for the development of an environmental impact statement prior to the application of rotenone or antimycin A (S.B. 1453, see State of Arizona Senate (2012b)) and urged the U.S. Environmental Protection Agency to deregister rotenone from use in the United States (S.B. 1009, see State of Arizona Senate (2012b)). Public safety considerations were fully evaluated by a multi-disciplined technical team of specialists that found no correlation between rotenone applications performed, according to product label instructions, and Parkinson's disease (Rotenone Review Advisory Committee 2012, pp. 24-25). Nonetheless, continued anxiety regarding the use of piscicides for conservation and management of fish communities leaves an uncertain future for this invaluable management tool. Should circumstances result in the discontinued practice of using piscicides for fish recovery and management, the likelihood of recovery for listed or sensitive aquatic vertebrates in Arizona, such as northern Mexican and narrow-headed gartersnakes, would be substantially reduced, if not eliminated outright.

We are supportive of the use of piscicides and consider the practice a vital and scientifically sound tool, the only tool in most circumstances, for reestablishing native fish communities and removing threats related to nonnative aquatic species in occupied northern Mexican and narrow-headed gartersnake habitat. However, it is equally important that effects of such treatments to these gartersnakes be evaluated during the project planning phase, specifically the amount of time a treated water body remains fishless post-treatment. The time period between rotenone applications and the subsequent restocking of native fish is contingent on two basic variables, the time it takes for piscicide levels to reach nontoxic levels and the level of certainty required to ensure that renovation goals and objectives have been met prior to restocking. Implementation of the latter consideration may vary from weeks, to months, to a year or longer, depending on the level of certainty required by project proponents. Carpenter and Terrell (2005, p. 14) reported that standard protocols, used by the Arizona Game and Fish Department for Apache trout renovations, required two applications of piscicide before repatriating native fish to a stream, waiting a season to see if the renovation was successful, and then continuing to renovate if necessary. Another recommendation of past protocols included a goal for the renovated water body to remain fishless an entire year before restocking (Carpenter and Terrell 2005, p. 14). At a minimum and according to our files, reaches of Big Bonito Creek, the West Fork Black River, West Fork Gila River, Iron Creek, Little Creek, Black Canyon, and O'Donnell Creek have all been subject to fish renovations using these or similarly accepted protocols (Carpenter and Terrell 2005; Table 6; Paroz and Probst 2009, p. 4; Hellekson 2012a, pers. comm.). Therefore, northern Mexican or narrow-headed gartersnake populations in these streams have likely been adversely affected, due to the eradication of a portion of, or their entire, prey base in these systems for varying periods of time. Big Bonito Creek was restocked with salvaged native fish shortly after renovation occurred. However, we are uncertain how long other stream reaches remained fishless post-treatment, but presume a minimum of weeks in each instance, and possibly a year or longer in some instances.

Future planning in fisheries management has identified several streams within the distribution of narrow-headed gartersnakes in New Mexico for potential fish barrier construction, for which piscicide applications are likely necessary. These streams include Little Creek, West Fork Gila River, Middle Fork Gila River, Turkey Creek, Saliz Creek, Dry Blue Creek, and the San Francisco River (Riley and Clarkson 2005, pp. 4-5, 7, 9, 12; Clarkson and Marsh 2012, p. 8; 2013, pp. 1, 4, 6). Of these, the Middle Fork Gila River and Turkey Creek appear to the most likely-chosen for renovation (Clarkson and Marsh 2013, p. 8). Mule Creek and Cienega Creek, both occupied by northern Mexican gartersnakes, as well as Whitewater Creek (occupied by narrow-headed gartersnakes) are under consideration but ultimately may not be chosen for renovation for undisclosed reasons (Clarkson and Marsh 2013, pp. 8-9).

In addition to fish, rotenone is toxic to amphibians in their gill-breathing,

larval life stages; adult forms tend to avoid treated water (Fontenot

et al.

1994, pp. 151-152). Rotenone has not been found to be directly toxic to aquatic snakes, but Fontenot

et al.

(1994, p. 152) suggested that effects from ingesting affected fish, frogs, or tadpoles may occur, but have not been adequately researched. The current standard operating procedures for piscicide application, as adopted nationally and provided in Finlayson

et al.

(2010, p. 23), provide guidance for assuring that non-target, baseline environmental conditions (the biotic community) are accounted for in assessing whether mitigation measures are necessary. This procedural protocol states, “Survival and recovery of the aquatic community may be demonstrated by sampling plankton, macroinvertebrates (aquatic insects, crustacea, leeches, and mollusks), and amphibians (frogs, tadpoles, and larval and adult salamanders)” (Finlayson

et al.

2010, p. 23). This protocol, adopted by the Arizona Game and Fish Department (see AGFD 2012), does not consider the effects of leaving a treated water body without a prey base for a sensitive species, such as the narrow-headed gartersnake, for extended periods of time. In fact, considerations for non-target aquatic reptiles, in general, are not mentioned anywhere in this broadly applied piscicide application protocol. Consequently, we have no reason to assume that effects to either northern Mexican or narrow-headed gartersnake populations from the partial or whole-scale removal of their prey base have been historically considered in piscicide applications, at least through 2006.

The potentially significant effects to northern Mexican or narrow-headed gartersnakes described above pertaining to piscicide application are largely historical in nature in Arizona, and new methodologies have been developed in Arizona to prevent adverse effects to gartersnake populations. As of 2012, a new policy was finalized by the Arizona Game and Fish Department that includes an early and widespread public notification and planning process that involves the approval of several decision-makers within four major stages: (1) Piscicide project internal review and approval; (2) preliminary planning and public involvement; (3) intermediate planning and public involvement; and (4) project implementation and evaluation (AGFD 2012, p. 3). Within the Internal Review and Approval stage of the process, sensitive, endemic, and listed species potentially impacted by the project must be identified (AGFD 2012, p. 13), such as northern Mexican or narrow-headed gartersnakes. In addition, the Arizona Game and Fish Department, through their Conservation and Mitigation Program developed as part of their sport fish stocking program through 2021, has committed to quickly restocking renovated streams that are occupied by either northern Mexican or narrow-headed gartersnakes (USFWS 2011, Appendix C).

Although significant efforts are generally made to salvage as many native fish as possible prior to treatment, logistics of holding fish for several weeks prior to restocking limit the number of individuals that can be held safely. Therefore, not every individual fish is salvaged, and native fish remaining in the stream are subsequently lost during the treatment. The number of fish subsequently restocked is, therefore, smaller than the number of fish that were present prior to the treatment. The full restoration of native fish populations to pre-treatment levels may take several years, depending on the size of the treated area and the size and maturity of the founding populations. Restocking salvaged fish in the fall may allow natural spawning and recruitment to begin in the spring, which would provide a more immediate benefit to resident gartersnake populations. With regard to New Mexico and Mexico, we are uncertain what measures have been considered in the past, or implemented currently, to prevent significant adverse impacts to northern Mexican or narrow-headed gartersnakes from piscicide applications.

Mechanical Methods

—In addition to chemical renovation techniques, mechanical methods using electroshocking equipment are often used in fisheries management, both for nonnative aquatic species removal and fisheries survey and monitoring activities that often occur in conjunction with piscicide treatments. Northern Mexican and narrow-headed gartersnakes often flee into the water as a first line of defense when startled. In occupied habitat, gartersnakes present within the water are often temporarily paralyzed from electrical impulses intended for fish, and are, therefore, readily detected by surveyors (Hellekson 2012a, pers. comm.). We are not aware of any research that has investigated potential short- or long-term consequences of such electrocutions to gartersnakes. In addition to the occupied streams noted above that have received piscicide applications (and therefore received electroshock surveys), Hellekson (2012, pers. comm.) reported narrow-headed gartersnakes being detected via electroshocking in the mainstem Gila River from Cliff Dwellings to Little Creek, the East Fork Gila River, Little Creek, Black Canyon, the Tularosa River, and Dry Blue Creek. Pettinger and Yori (2011, p. 11) reported detecting two narrow-headed gartersnakes as a result of electroshocking in the West Fork Gila River. Thus, electroshock surveys may be a source of additional data related to the occurrence and distribution of both northern Mexican and narrow-headed gartersnakes.

Trapping methods are also used in fisheries surveys, for other applications in aquatic species management, and for the collection of live baitfish in recreational fishing. One such common method to study aquatic or semi-aquatic wildlife (including populations of aquatic snakes such as gartersnakes) is through the use of self-baiting wire minnow traps. When used to monitor gartersnake populations, wire minnow traps are anchored to vegetation, logs, etc., along the shoreline (in most applications) and positioned so that half to one-third of the trap, along its lateral line, is above water surface to allow snakes to surface for air. These traps are then checked according to a predetermined schedule.

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