Tuesday, November 25, 2008
Part III
Department of the Interior Fish and Wildlife Service
50 CFR 17 Endangered and Threatened Wildlife and Plants; 12-Month Finding on a Petition To List the Northern Mexican Gartersnake (Thamnophis eques megalops) as Threatened or Endangered With Critical Habitat; Proposed Rule
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DEPARTMENT OF THE INTERIOR FWS–R2–ES–2008–0065. Supporting March 1, 2004. In that letter, we also documentation we used in preparing advised the petitioners that, due to Fish and Wildlife Service this finding is available for public funding constraints in fiscal year (FY) inspection, by appointment, during 2004, we would not be able to begin 50 CFR Part 17 normal business hours at the U.S. Fish processing the petition at that time. [FWS–R2–ES–2008–0065; MO 9221050083– and Wildlife Service, Arizona Ecological Previous Federal Actions B2] Services Office, 2321 West Royal Palm Road, Suite 103, Phoenix, AZ 85021– The Mexican gartersnake Endangered and Threatened Wildlife 4951. Please submit any new (Thamnophis eques) (which included and Plants; 12-Month Finding on a information, materials, comments, or the subspecies megalops) was placed on Petition To List the Northern Mexican questions concerning this finding to the the list of candidate species as a Gartersnake (Thamnophis eques above address. Category 2 species in 1985 (50 FR 37958). Category 2 species were those megalops) as Threatened or FOR FURTHER INFORMATION CONTACT: for which existing information indicated Endangered with Critical Habitat Steve Spangle, Field Supervisor, that listing was possibly appropriate, Arizona Ecological Services Office (see AGENCY: Fish and Wildlife Service, but for which substantial supporting ADDRESSES), telephone 602–242–0210. If Interior. biological data to prepare a proposed you use a telecommunications device rule were lacking. In the 1996 Candidate ACTION: Notice of 12-month petition for the deaf (TDD), please call the Notice of Review (February 28, 1996; 61 finding. Federal Information Relay Service FR 7596), the use of Category 2 (FIRS) at 800–877–8339. SUMMARY: We, the U.S. Fish and candidates was discontinued, and the Wildlife Service (Service), announce a SUPPLEMENTARY INFORMATION: northern Mexican gartersnake was no 12-month finding on a petition to list Background longer recognized as a candidate. the northern Mexican gartersnake On May 17, 2005, the petitioners filed (Thamnophis eques megalops) as Section 4(b)(3)(B) of the Act (16 a complaint for declaratory and threatened or endangered with critical U.S.C. 1531 et seq.), requires that, for injunctive relief, challenging our failure habitat under the Endangered Species any petition containing substantial to issue a 90-day finding in response to Act of 1973, as amended (Act). The scientific and commercial information the petition as required by 16 U.S.C. petitioners provided three listing indicating that listing may be warranted, 1533(b)(3)(A) and (B). In a stipulated options for consideration by the Service: we make a finding within 12 months of settlement agreement, we agreed to (1) Listing the U.S. population as a the date of receipt of the petition on submit a 90-day finding to the Federal Distinct Population Segment (DPS); (2) whether the petitioned action is: (a) Not Register by December 16, 2005, and if listing Thamnophis eques megalops warranted, (b) warranted, or (c) substantial, submit a 12-month finding throughout its range in the United States warranted, but immediate proposal of a to the Federal Register by September and Mexico based on its rangewide regulation implementing the petitioned 15, 2006 (Center for Biological Diversity status; or (3) listing Thamnophis eques action is precluded by other pending v. Norton, CV–05–341–TUC–CKJ megalops throughout its range in the proposals to determine whether species (D. Az)). The settlement agreement was United States and Mexico based on its are threatened or endangered, and signed and adopted by the District Court status in the United States. On the basis expeditious progress is being made to of Arizona on August 2, 2005. of the best scientific and commercial add or remove qualified species from On December 13, 2005, we made our information available, we find that the Lists of Endangered and Threatened 90-day finding that the petition listing the northern Mexican gartersnake Wildlife and Plants. Section 4(b)(3)(C) of presented substantial scientific as threatened or endangered throughout the Act requires that we treat a petition information indicating that listing the its range in the United States and for which the requested action is found northern Mexican gartersnake Mexico, based on its rangewide status, to be warranted but precluded as though (Thamnophis eques megalops) may be is warranted under the Act, due to the resubmitted on the date of such finding; warranted, but we did not discuss the present or threatened destruction, that is, requiring a subsequent finding to applicability of any of the three listing modification or curtailment of its be made within 12 months. We must scenarios that were provided in the habitat; predation; and the inadequacy publish these 12-month findings in the petition. The finding and our initiation of existing regulatory mechanisms. Federal Register. of a status review was published in the Currently, listing is precluded by higher On December 19, 2003, we received a Federal Register on January 4, 2006 (71 priority actions to amend the Lists of petition dated December 15, 2003, FR 315). Endangered and Threatened Wildlife requesting that we list the northern On September 26, 2006, we published and Plants. Upon publication of this 12- Mexican gartersnake as threatened or a 12-month finding that listing of the month petition finding, the northern endangered, and that we designate northern Mexican gartersnake was not Mexican gartersnake will be added to critical habitat concurrently with the warranted because we determined that our candidate species list. We will listing. The petition, submitted by the not enough information on the develop a proposed rule to list the Center for Biological Diversity, was subspecies’ status and threats in Mexico northern Mexican gartersnake as our clearly identified as a petition for a was known at that time (71 FR 56227). priorities allow. Any determination on listing rule and contained the names, On November 17, 2007, the petitioners critical habitat will be made during signatures, and addresses of the filed a complaint for declaratory and development of the proposed rule. requesting parties. Included in the injunctive relief pursuant to section 11 petition was supporting information of the Act (16 U.S.C. 1540), seeking to DATES: The finding announced in this regarding the species’ taxonomy and set aside the 12-month finding. document was made on November 25, ecology, historical and current Additionally, a formal opinion was 2008. distribution, present status, and actual issued by the Solicitor of the ADDRESSES: This finding is available on and potential causes of decline. We Department of the Interior, ‘‘The the Internet at http:// acknowledged the receipt of the petition Meaning of In Danger of Extinction www.regulations.gov at Docket Number in a letter to Mr. Noah Greenwald, dated Throughout All or a Significant Portion
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of Its Range’’ (U.S. DOI 2007), which detailed species description can be name changes, including many species provides further guidance on how to found in our 2006 12-month finding for under the genus Rana to Lithobates, and conduct a detailed analysis of whether this species (71 FR 56227), or by many species under the genus Bufo to a species is in danger of extinction reviewing Rosen and Schwalbe (1988, Anaxyrus. Crother (2008, pp. 2–12), throughout a significant portion of its p.4), Rossman et al. (1996, pp. 171–172), Committee Chair for the Standard range. In December 2007, the Service or Manjarrez and Garcia (1993, pp. 1–5). English and Scientific Names withdrew the September 26, 2006, Taxonomy. The northern Mexican Committee, adopted these scientific 12-month finding to consider the new gartersnake is a member of the family name changes. However, these ‘‘Significant Portion of the Range’’ Colubridae and subfamily Natricinae taxonomic revisions have not escaped policy. In a stipulated settlement (harmless live-bearing snakes) (Lawson significant scrutiny in the scientific agreement with the petitioners, we et al. 2005, p. 596). The taxonomy of the literature. Weins (2007, pp. 55–56) agreed to submit a new 12-month genus Thamnophis has a complex criticized the methodologies and finding to the Federal Register by history, partly because many of the analysis of Frost et al. (2006, pp. 9–11). November 17, 2008 (Center for species are similar in appearance and Subsequently, Frost et al. (2008, pp. Biological Diversity v. Kempthorne, scutelation (arrangement of scales), but 385–395) rebutted these criticisms. CV–07–596–TUC–RCCJ (D. Az)). The also because many of the early museum Throughout this finding, we continue to settlement agreement was signed and specimens were in such poor and faded use the genera Rana and Bufo to adopted by the District Court of Arizona condition that it was difficult to study maintain taxonomic familiarity among on June 18, 2008. them (Conant 2003, p. 6). the interested parties, retain consistency This notice constitutes a new 12- In recent history and prior to 2003, in the Federal Register with respect to month finding for the petition to list the Thamnophis eques was considered to notices regarding the northern Mexican northern Mexican gartersnake as have three subspecies, T. e. eques, T. e. gartersnake, and allow ample threatened or endangered. The megalops, and T. e. virgatenuis opportunity for peer review and petitioners described three potentially (Rossman et al. 1996, p. 175). In 2003, deliberation in the scientific community listable entities of gartersnake for an additional seven new subspecies with respect to the findings of Frost et consideration by the Service: (1) Listing were identified under T. eques: (1) T. e. al. (2006, pp. 9–11). the U.S. population as a Distinct cuitzeoensis; (2) T. e. patzcuaroensis; (3) Habitat. Throughout its rangewide Population Segment (DPS); (2) listing T. e. inspiratus; (4) T. e. obscurus; (5) T. distribution, the northern Mexican Thamnophis eques megalops e. diluvialis; (6) T. e. carmenensis; and gartersnake occurs at elevations from throughout its range in the United States (7) T. e. scotti (Conant 2003, p. 3). 130 to 8,497 feet (ft) (40 to 2,590 meters and Mexico based on its rangewide Common names were not provided, so (m)) (Rossman et al. 1996, p. 172). The status; or (3) listing Thamnophis eques in this finding, we use the scientific northern Mexican gartersnake is a megalops throughout its range in the name for all subspecies of Mexican riparian obligate (restricted to riparian United States and Mexico based on its gartersnake other than the northern areas when not engaged in dispersal status in the United States. Because we Mexican gartersnake. These seven new behavior) and occurs chiefly in the found that listing the northern Mexican subspecies were described based on following general habitat types: (1) gartersnake rangewide was warranted, morphological differences in coloration Source-area wetlands (e.g., cienegas there was no need to conduct any and pattern; have highly restricted (mid-elevation wetlands with highly further analysis of the remaining two distributions; and occur in isolated organic, reducing (basic or alkaline) options, which are smaller geographic wetland habitats within the soils), stock tanks (small earthen entities and are subsumed by the mountainous Transvolcanic Belt region impoundment), etc.); (2) large-river rangewide listing. of southern Mexico, which contains the riparian woodlands and forests; and (3) highest elevations in the country streamside gallery forests (as defined by Biology (Conant 2003, pp. 7–8). There are no well-developed broadleaf deciduous Species Description. The northern known challenges within the scientific riparian forests with limited, if any, Mexican gartersnake ranges in color literature of the validity of current herbaceous ground cover or dense grass) from olive to olive-brown or olive-gray taxonomy of any of the 10 subspecies of (Hendrickson and Minckley 1984, p. with three stripes that run the length of T. eques. A more detailed description of 131; Rosen and Schwalbe 1988, pp. 14– the body, the middle of which darkens the taxonomy of the northern Mexican 16; Arizona Game and Fish Department towards the tail. It may occur with other gartersnake is found in our September 2001). Additional information on the native gartersnake species and can be 26, 2006 12-month finding for this habitat requirements of the northern difficult for people without species (71 FR 56227). Additional Mexican gartersnake within the United herpetological expertise to identify. The information regarding this species’ States and Mexico can be found in our snake may reach a maximum known taxonomy can be found in De Queiroz 2006 12-month finding for this species length of 44 inches (in) [(112 et al. (2002, P. 323), De Queiroz and (71 FR 56227) and in Rosen and centimeters (cm)]. The pale yellow to Lawson (1994, p. 217), Rossman et al. Schwalbe (1988, pp. 14–16), Rossman et light-tan lateral stripes distinguish the (1996, pp. xvii–xviii, pp. 171–175), al. (1996, p. 176), McCranie and Wilson northern Mexican gartersnake from Rosen and Schwalbe (1988, pp. 2–3), (1987, pp. 11–17), and Cirett-Galan other sympatric (co-occurring) Liner (1994, p. 107), and Crother (2008, (1996, p. 156). gartersnake species because a portion of p. 63). Behavior, Prey Base, and the lateral stripe is found on the fourth On many occasions throughout this Reproduction. The northern Mexican scale row, while it is confined to lower finding, we discuss the status of and gartersnake is surface active at ambient scale rows for other species. Paired threats to several prey species of the temperatures ranging from 71 degrees black spots extend along the olive northern Mexican gartersnake, Fahrenheit (°F) to 91 °F (22 degrees dorsolateral fields (region adjacent to including anuran (frog and toad) species Celsius (°C) to 33 °C) and forages along the top of the snake’s back) and the of the genera historically known as the banks of waterbodies. Rosen (1991, olive-gray ventrolateral fields (region Rana and Bufo (true frogs and true pp. 308–309) found that northern adjacent to the area of the snake’s body toads, respectively). Frost et al. (2006, Mexican gartersnakes spent in contact with the ground). A more pp. 9–11) proposed several taxonomic approximately 60 percent of their time
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moving, 13 percent of their time basking fed primarily upon aquatic vertebrates p. 40; Nickerson and Mays 1970, p. 503; on vegetation, 18 percent of their time (fishes, frogs, and larval salamanders) Bradley 1986, p. 67; Rosen and basking on the ground, and 9 percent of and leeches, whereas smaller snakes fed Schwalbe 1988, Appendix I; 1995, p. their time under surface cover; body primarily upon earthworms and leeches 452; 1997, pp. 16–17; Holm and Lowe temperatures ranged from 24–33 °C (75– (Marcı´as-Garcı´a and Drummond 1988, 1995, pp. 27–35; Sredl et al. 1995b, p. 91 °F) and averaged 28 °C (82 °F), which p. 131). Marcı´as-Garcı´a and Drummond 2; 2000, p. 9; Rosen et al. 2001, is lower than other, similar species with (1988, p. 130) also found that Appendix I; Holycross et al. 2006, pp. comparable habitat and prey parturition (birth) of neonatal T. eques 1–2, 15–51; Brennan and Holycross preferences. Rosen (1991, p. 310) tended to coincide with the annual peak 2006, p. 123; Radke 2006; Rosen 2006; suggested that lower preferred body density of annelids (earthworms and Holycross 2006). temperatures exhibited by northern leeches). Positive correlations were also Historically, the northern Mexican Mexican gartersnakes may be due to made with respect to capture rates gartersnake had a limited distribution in both (1) their tendency to occupy (which are correlated with population New Mexico that consisted of scattered cienega-like habitat where warm size) of T. eques to lake levels and to locations throughout the Gila and San ambient temperatures are relatively prey scarcity; that is, when lake levels Francisco headwater drainages in Grant unavailable; and, (2) their tendency to were low and/or prey species scarce, and western Hidalgo Counties (Price remain in dense cover. Mexican gartersnake capture rates 1980, p. 39; Fitzgerald 1986, Table 2; The northern Mexican gartersnake is declined (Marcı´as-Garcı´a and Degenhardt et al. 1996, p. 317; an active predator and is believed to Drummond 1988, p. 132). This indicates Holycross et al. 2006, pp. 1–2). heavily depend upon a native prey base the importance of available water and One record for the northern Mexican (Rosen and Schwalbe 1988, pp. 18, 20). an adequate prey base to maintaining gartersnake exists for the State of Northern Mexican gartersnakes forage viable populations of Mexican Nevada, opposite Fort Mohave, in Clark generally along vegetated banklines, gartersnakes. Marcı´as-Garcı´a and County along the shore of the Colorado searching for prey in water and on land, Drummond (1988, p. 133) found that River (De Queiroz and Smith 1996, p. using different strategies (Alfaro 2002, while certain prey items were positively 155). The species may have occurred p. 209). Generally, its diet consists associated with size classes of snakes, historically in the lower Colorado River predominantly of amphibians and the largest of specimens consume any region of California, although we were fishes, such as adult and larval native prey available. unable to verify any museum records for leopard frogs (e.g., lowland leopard frog Sexual maturity in northern Mexican California. Any populations of northern (Rana yavapaiensis) and Chiricahua gartersnakes occurs at 2 years of age in Mexican gartersnakes that may have leopard frog (Rana chiricahuensis)), as males and at 2 to 3 years of age in historically occurred in either Nevada or well as juvenile and adult native fish females (Rosen and Schwalbe 1988, pp. California likely pertained directly to species (e.g., Gila topminnow 16–17). Northern Mexican gartersnakes the Colorado River and are extirpated. (Poeciliopsis occidentalis occidentalis), are ovoviviparous (eggs develop and Within Mexico, northern Mexican desert pupfish (Cyprinodon hatch within the oviduct of the female). gartersnakes historically occurred macularius), Gila chub (Gila Mating occurs in April and May within the Sierra Madre Occidental and intermedia), and roundtail chub (Gila followed by the live birth of between 7 the Mexican Plateau in the Mexican robusta)) (Rosen and Schwalbe 1988, p. and 26 newborns (newly born states of Sonora, Chihuahua, Durango, 18). Auxiliary prey items may also individuals) (average is 13.6) in July and Coahila, Zacatecas, Guanajuato, Nayarit, include young Woodhouse’s toads (Bufo August (Rosen and Schwalbe 1988, p. Hidalgo, Jalisco, San Luis Potosı´, woodhousei), treefrogs (Family Hylidae), 16). Unlike other gartersnake species, Aguascalientes, Tlaxacala, Puebla, earthworms, deermice (Peromyscus which typically breed annually, Me´xico, Veracruz, and Quere´taro, spp.), lizards of the genera Aspidoscelis approximately half of the sexually comprising approximately 85 percent of and Sceloporus, larval tiger salamanders mature females within a population of the total rangewide distribution of the (Ambystoma tigrinum), and leeches northern Mexican gartersnake reproduce species (Conant 1963, p. 473; 1974, pp. (Gregory et al. 1980, pp. 87, 90–92; in any one season (Rosen and Schwalbe 469–470; Van Devender and Lowe 1977, Rosen and Schwalbe 1988, p. 20; Holm 1988, p. 17). This may have negative p. 47; McCranie and Wilson 1987, p. 15; and Lowe 1995, pp. 30–31; Degenhardt implications for the species’ ability to Rossman et al. 1996, p. 173; Lemos- et al. 1996, p. 318; Rossman et al. 1996, rebound in isolated populations facing Espinal et al. 2004, p. 83). p. 176; Manjarrez 1998). To a much threats such as nonnative species, Status in the United States. lesser extent, this snake’s diet may habitat modification or destruction, and Variability in survey design and effort include nonnative species, including other perturbations. Low birth rates will makes it difficult to compare population larval and juvenile bullfrogs, and impede recovery of such populations by trends among sites and between mosquitofish (Gambusia affinis) accentuating the effects of these threats. sampling periods. Thus, for each of the (Holycross et al. 2006, p. 23). Venegas- sites considered in our analysis, we Distribution Barrera and Manjarrez (2001, p. 187) have attempted to translate and quantify reported the first observation of a snake Historical Distribution. Within the search and capture efforts into in the natural diet of any species of United States, the northern Mexican comparable units (i.e., person-search Thamnophis after documenting the gartersnake historically occurred hours and trap-hours) and have consumption by a Mexican gartersnake predominantly in Arizona at elevations cautiously interpreted those results. of a Mexican alpine blotched ranging from 130 to 6,150 ft (40 to 1,875 Given the data provided, it is not gartersnake (Thamnophis scalaris). m) in elevation. It was generally found possible to determine population Marcı´as-Garcı´a and Drummond (1988, where water was relatively permanent densities at the sites. pp. 129–134) sampled the stomach and supported suitable habitat. The A detailed status of the northern contents of Mexican gartersnakes and northern Mexican gartersnake Mexico gartersnake in the United States the prey populations at (ephemeral) historically occurred in every county and Mexico can be found in our 2006 Lake Tecocomulco, Hidalgo, Mexico. within Arizona, within several 12-month finding (71 FR 56227) and in Field observations indicated with high perennial or intermittent drainages and Holycross et al. (2006, p. 12); Rosen and statistical significance that larger snakes disassociated wetlands (Woodin 1950, Schwalbe (1988, Appendix 1); Rosen et
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al. (2001, pp. 21–22, Appendix 1); Conservation Working Group (GCWG) trap-hours per snake) in 2004 and 2005 d’Orgeix (2008); Holm and Lowe (1995, 2008, pp. 1–10). Servoss et al. (2007, p. (Holycross et al. 2006, pp. 41–44; pp. 27–35). Subsequent to our 2006 12- 4) captured one juvenile northern Wallace et al. 2008, pp. 243–244). month finding, we have obtained and Mexican gartersnake by hand after 27 Wallace et al. (2008, pp. 243–244) analyzed additional information person search-hours and 1,000 trap- suggest northern Mexican gartersnakes pertinent to the status of the northern hours of effort. in Tonto Creek persist in low densities Mexico gartersnake and present it Due to limited success in collecting and raise the possibility that below. the species in 2007, in 2008, the recruitment (the process by which Scotia Canyon was the last area Arizona Game and Fish Department individuals within a population achieve intensively resurveyed by Rosen et al. contracted with a recognized reptile and reproductive maturity) may be in (2001, pp. 15–16). In comparing capture amphibian researcher familiar with the decline because only adult and newborn rates from Holm and Lowe (1995, pp. area to collect specimens for captive specimens were captured, with no 27–35), northern Mexican gartersnake propagation (GCWG 2008, pp. 1–10). intermediate age classes observed. populations in this area appear to have The herpetologist trapped a single The population of northern Mexican declined from 1980–1982, to low juvenile northern Mexican gartersnake gartersnakes along the Verde River capture rates in 1993, and even lower in 3,612 trap-hours and 104 person within the Verde Valley of Yavapai capture rates in 2000 (Boyarski 2008c, p. search-hours of effort (Caldwell 2008a, County is presumed to remain as a low- 1). In 2008, a multi-party effort was 2008b). density population. Approximately 15 initiated within Scotia Canyon, The wildlife biologist for the Bureau individuals, including agency personnel including the Peterson Ranch Pond and of Land Management (BLM) Tucson and private citizens, surveyed the Verde vicinity, to eradicate bullfrogs as well as Field Office (who has conducted fish River within the Verde Valley record observations of Chiricahua sampling at the Las Cienegas National (including Dead Horse Ranch State leopard frogs or northern Mexican Conservation Area since 1998) Park) for the purpose of collecting 5 gartersnakes (Frederick 2008, 2008b). expressed concerns for the apparent Mexican gartersnakes for captive These efforts occurred in the same area population decline of northern Mexican propagation in 2007 (GCWG 2007, p. 2). investigated by Holm and Lowe (1995, gartersnakes in this area. Several fish Approximately 120 person-search hours pp. 27–35) and Rosen et al. (2001, pp. sampling techniques he employs are resulted in no observations of northern 15–16). After many surveys of also used specifically to sample aquatic Mexican gartersnakes (GCWG 2007, p. herpetofauna (reptiles and amphibians) snake species such as the northern 2). Haney et al. (2008, p. 61) declared in this area to identify the presence of Mexican gartersnake. Simms (2008) the northern Mexican gartersnake nearly bullfrogs for eradication, a single, large stated that seining and hoop netting at lost from the Verde River. adult northern Mexican gartersnake was 40 locations, as well as visual surveys A population of northern Mexican observed, the first in over 8 years of of this area performed in 2008, have gartersnakes that remains at the Arizona informal surveys at this site (Frederick yielded no observations of Mexican Game and Fish Department’s Page 2008b), which is frequently visited by gartersnakes. Springs and Bubbling Ponds fish biologists. This observation suggests The data from 2007 and 2008 confirm hatcheries (hatcheries), located adjacent that the species continues to occur in that this formerly stable population at to Oak Creek, upstream of its confluence the upper Scotia Canyon area, but, given the Las Cienegas National Conservation with the Verde River, represents the the extensive survey effort, it occurs in Area is experiencing significant highest density population in Arizona exceptionally low densities and no declines, may no longer be viable, and and potentially the last remaining viable longer represents a stable population could become extirpated in the near- population in the United States. because of problems with reproduction term. In 2007 and 2008, more than 2,300 Boyarski (2008b, pp. 1–10) summarizes and survivorship that exist with trap-hours were required per snake the first (2007) field season of a northern populations comprised of very low captured (Caldwell 2008a, 2008b; Mexican gartersnake monitoring project numbers of individuals. Servoss et al. 2007, p. 1–12), compared at the hatcheries, which had the A significant amount of survey effort with Rosen and Caldwell’s (2004, p. 21 objective of establishing the baseline for northern Mexican gartersnakes was Table 2) capture rates of 561 trap-hours population demographics from which to conducted at the Las Cienegas National per snake in 2002 and 2003. This is a launch future investigations (Boyarski Conservation Area (Cienega Creek and more than four-fold increase in the 2008b, p. 4). Although several capture Empire Cienega) from 2002–2008. effort needed to capture northern techniques were employed, trapping During the 2002 and 2003 field seasons, Mexican gartersnakes. was the most effective by far. In total, 52 Rosen and Caldwell (2004, pp. 1–52) The recently documented population individual northern Mexican conducted an in-depth assessment of of northern Mexican gartersnakes within gartersnakes were captured in 2007; 42 the riparian herpetofaunal community Tonto Creek is the only known from Bubbling Ponds, 8 from Page of this area and in 11,784 trap-hours population that remains from the Salt Springs, and 2 from the adjacent Oak captured by hand and trap, 29 northern River Basin (the status of the species in Creek (Boyarski 2008b, p. 5). In total, Mexican gartersnakes that were marked the basin on the White Mountain 19,457 trap-hours captured 56 northern and released. Twenty-one northern Apache and San Carlos Apache Mexican gartersnakes (including 7 Mexican gartersnakes were trapped, reservations remains unknown). recaptures), which equates to 347 trap- which equates to 561 trap-hours per Wallace et al. (2008, pp. 243–244) hours per capture (Boyarski 2008b, p. 6). snake. In 2004, Rosen and Caldwell documented the first record of northern As this was the first year to acquire (2004, p. 21) considered the species to Mexican gartersnakes from the Tonto population data for northern Mexican be ‘‘widely distributed, though perhaps Creek watershed in Gila County, from a gartersnakes within the hatcheries, reduced in abundance’’ in this area. specimen that was observed in the road population trends at these sites cannot In 2007 and 2008, significant effort to (killed by a vehicle) on State Route 188 be determined. However, hatchery collect northern Mexican gartersnakes in 1995. Seventeen individual northern personnel stated that northern Mexican was given to this same area using Mexican gartersnakes were gartersnakes are not observed as similar techniques as Rosen and subsequently captured in Tonto Creek frequently and do not appear to be as Caldwell (2004) (Gartersnake with 20,444 trap-hours of effort (1,202 common as they once were at these sites
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(Boyarski 2008b, p. 8). While not within northern Mexican gartersnake In New Mexico, the following associated with a scientific study, this populations that have been affected by historical populations are considered statement by hatchery personnel, who nonnative species. It is widely believed extirpated: (1) Mule Creek; (2) the Gila spend most of their time in the that recruitment of northern Mexican River, 5 miles (mi) (8 kilometers (km)) immediate vicinity of occupied habitat, gartersnakes may be significantly east of Virden; (3) Spring Canyon; (4) is of special concern because it impeded by nonnative predation on the the West Fork Gila River at Cliff illustrates the potential that long-term neonate and juvenile age classes. Dwellings National Monument; (5) the declines may have been occurring at the Individuals that survive past these age Tularosa River at its confluence with the hatchery although potential declines classes are likely to have increased San Francisco River; (6) the San can not be quantified. survivorship, in part by foraging on the Francisco River at Tub Spring Canyon; Sonoita Creek in Santa Cruz County nonnative species that preyed upon (7) Little Creek at Highway 15; (8) the in southern Arizona was a historical them during their younger age classes. Middle Box of Gila River at Ira Ridge; location for northern Mexican These population-level observations (9) Turkey Creek; (10) Negrito Creek; gartersnakes. Turner (2006, pp. 1–21) have been made in several populations and (11) the Rio Mimbres (Fitzgerald found no northern Mexican gartersnakes including Scotia Canyon (Holm and 1986, Table 2; Painter 2005, 2006; 2008; in a herpetological inventory conducted Lowe 1995, p. 34), Tonto Creek (Wallace Cotton 2008; Kindscher In Prep., pp. from April through September 2006, in et al. 2008, pp. 243–244), and the San 1–26). the Sonoita Creek State Natural Area. Bernardino National Wildlife Refuge Conversely, our review of the best The last record of a northern Mexican (Rosen and Schwalbe 1988, p. 18). available information indicates the gartersnake in this area was in 1974 and northern Mexican gartersnake likely Our analysis of the best available data the subspecies was not found during occurs in a fraction of its former range on the status of the northern Mexican Turner’s 204-person-search-hour, 5,472- in Arizona. We define populations as gartersnake distribution in the United trap-hour survey effort (Turner 2006, ‘‘likely occurring’’ when the species is States indicates that its distribution has pp. 3, 9). Crayfish, bullfrogs, and expected to reliably occur in been significantly reduced, and it is nonnative fish were observed by Turner appropriate habitat as supported by likely extirpated from a large portion of (2006, p. 10) throughout the riparian recent museum records and/or recent its historical distribution within the area of the study area, as was evidence (i.e., less than 10 years) reliable United States. We define a population of improper livestock grazing. observations. The perennial or In our 2006 12-month finding for this as ‘‘likely extirpated’’ when there have intermittent stream reaches and species, we specified that the last been no northern Mexican gartersnakes disassociated wetlands where we known observation of the northern reported for a decade or longer at a site conclude northern Mexican gartersnakes Mexican gartersnake in New Mexico within the historical distribution of the remain include: (1) The Santa Cruz occurred in 1994 on private land species, despite survey efforts, and there River/Lower San Rafael Valley (Painter 2000, p. 36, Painter 2005). In is no expectation of natural recovery at (headwaters downstream to the 2007, we became aware of a single the site due to the presence of known or International Border); (2) the Verde photo-vouchered record of a northern strongly suspected causes of extirpation. River from the confluence with Fossil Mexican gartersnake in New Mexico. The perennial or intermittent stream Creek upstream to Clarkdale; (3) Oak The specimen was discovered and reaches and disassociated wetlands (i.e., Creek at Page Springs; (4) Tonto Creek photo-vouchered in August 2002, stock tanks, ponds, cienegas, etc.) where from the mouth of Houston Creek observed in a debris pile along the Gila the northern Mexican gartersnake has downstream to Roosevelt Lake; (5) River off Highway 180 in Grant County, likely been extirpated in Arizona Cienega Creek from the headwaters New Mexico (Hill 2007). Subsequent include: (1) The Gila River; (2) the downstream to the ‘‘Narrows’’ just searches for northern Mexican Lower Colorado River from Davis Dam downstream of Apache Canyon; (6) gartersnakes were conducted in the to the International Border; (3) the San Pantano Wash (Cienega Creek) from same vicinity in 2006 and 2007, but no Pedro River; (4) the Santa Cruz River Pantano downstream to Vail; (7) individuals were observed (Hill 2007). downstream from the International Appleton-Whittell Research Ranch and In our 2006 finding (71 FR 56227), we Border at Nogales; (5) the Salt River; (6) vicinity near Elgin; and (8) Red Rock considered the northern Mexican the Rio San Bernardino from Canyon east of Patagonia (Rosen et al. gartersnake as extirpated from New International Border to headwaters at 2001, Appendix I; Caldwell 2005; Mexico. In consideration of: (1) A single Astin Spring (San Bernardino National Brennan and Holycross 2006, p. 123; observation of the species in New Wildlife Refuge); (7) the Agua Fria Holycross 2006; Holycross et al. 2006, Mexico within the last 14 years that River; (8) the Verde River upstream of pp. 15–51, 66; Rosen 2006; Jones 2008a). occurred in 2002; (2) 2 years of survey Clarkdale; (9) the Verde River from the The current status of the northern effort in 2006 and 2007 within the Gila confluence with Fossil Creek Mexican gartersnake is unknown in River in the area of the 2002 observation downstream to its confluence with the several areas within Arizona and New by Hill (2007); and (3) additional survey Salt River; (10) Tanque Verde Creek in Mexico where the species is known to effort of historical habitat for the species Tucson; (11) Rillito Creek in Tucson; have historically occurred. We base this in New Mexico in 2007, we consider the (12) Agua Caliente Spring in Tucson; determination primarily on historical status of the northern Mexican (13) Potrero Canyon/Springs; (14) museum records for locations where gartersnake in the Gila River at the Babocamari Cienega; (15) Barchas survey access is restricted, survey data Highway 180 crossing in New Mexico as Ranch, Huachuca Mountain bajada; (16) are unavailable or insufficient, and/or unknown at this time (Painter 2008; Parker Canyon Lake and tributaries in current threats could preclude Cotton 2008; Kindscher In Prep., pp. 1– the Canelo Hills; and (17) Oak Creek at occupancy. The perennial or 26). All other historical locations of the Midgley Bridge (Rosen and Schwalbe intermittent stream reaches and northern Mexican gartersnake in New 1988, pp. 25–26, Appendix I; 1997, pp. disassociated wetlands where the status Mexico are considered extirpated 16–17; Rosen et al. 2001, Appendix I; of the northern Mexican gartersnake (Painter 2005). Brennan and Holycross 2006, p. 123; remains uncertain include: (1) The General concerns within the scientific Holycross 2006; Holycross et al. 2006, downstream portion of the Black River community exist for age class structure pp. 15–51, 66; Radke 2006; Rosen 2006). drainage from the Paddy Creek
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confluence; (2) the downstream portion northern Mexican gartersnake has also surveys, research, and other pertinent of the White River drainage from the been lost from these sites. Contreras information for that country. We can confluence of the East and North forks; Balderas and Lozano (1994, p. 381) determine that there have been (3) Big Bonito Creek; (4) Lake O’Woods stated that several streams and rivers important large-scale losses of northern near Lakeside; (5) Spring Creek above throughout Mexico and within the Mexican gartersnake habitat, including the confluence with Oak Creek; (6) Bog distribution of the northern Mexican surface waters such as rivers, streams, Hole Wildlife Area; (7) Upper 13 Tank, gartersnake have also dried up or wetlands, and springs, that certainly Patagonia Mountain bajada; (8) become intermittent due to overuse of have affected gartersnake populations. Babocamari River; (9) Upper Scotia surface and groundwater supplies. We can also determine that, where local Canyon in the Huachuca Mountains; Ramirez Bautista and Arizmendi (2004, surveys have been conducted, northern (10) Arivaca Cienega; and, (11) Gila p. 3) stated that the principal threats to Mexican gartersnakes have been River at Highway 180 (in New Mexico) northern Mexican gartersnake habitat in extirpated or are declining (Manjarrez (Rosen and Schwalbe 1988, Appendix I; Mexico include the drying of wetlands. 2008). Rosen et al. 2001, Appendix I; Brennan Because this has decreased the amount and Holycross 2006, p. 123; Holycross of habitat and the aquatic prey base of Summary of Factors Affecting the 2006; Holycross et al. 2006, pp. 15–51; the snake, we conclude that the Northern Mexican Gartersnake Rosen 2006). northern Mexican gartersnake has likely In summary, based upon our analysis declined at these sites. Section 4 of the Act (16 U.S.C. 1533), of the best available scientific and Burger (2008) provides a preliminary and implementing regulations at 50 CFR commercial data, we conclude that the data set of survey effort for Mexican 424, set forth procedures for adding northern Mexican gartersnake has been gartersnakes (Thamnophis eques), species to the Federal Lists of extirpated from approximately 90 southern Durango spotted gartersnakes Endangered and Threatened Wildlife percent of its historical distribution in (T. nigronuchalis), and narrow-headed and Plants. Under section 4(a)(1) of the the United States. gartersnakes (T. rufipunctatus) from the Act, we may list a species on the basis Status in Mexico. Determining the United States and Mexico through 2007 of any of five factors, as follows: (A) The status and current distribution of the (T. nigronuchalis only occurs in present or threatened destruction, northern Mexican gartersnake in Mexico Mexico). The Burger (2008) data set modification, or curtailment of its is difficult because of the lack of large- provides information from surveys of 17 habitat or range; (B) overutilization for scale surveys, research, and other stream systems in the Mexican states of commercial, recreational, scientific, or pertinent information. We can Durango and southern Chihuahua along educational purposes; (C) disease or determine that there have been the Sierra Madre Occidental during June predation; (D) the inadequacy of important large-scale losses of northern 2007. Mexican gartersnakes were existing regulatory mechanisms; or (E) Mexican gartersnake habitat, and that, at observed at 5 of the 17 sites visited; other natural or manmade factors least locally, northern Mexican however, specimens were not identified gartersnake populations have been to subspecies, and some sites visited affecting its continued existence. In extirpated or are declining. We relied, in may not have been within the historical making this finding, information part, on information that addresses the distribution of the northern Mexican regarding the status of, and threats to, status of both riparian and aquatic gartersnake. Individuals observed from the northern Mexican gartersnake in biological communities that are habitat locations in southern Durango were relation to the five factors provided in for the northern Mexican gartersnake likely T. e. virgatenuis, rather than the section 4(a)(1) of the Act is discussed and the status of native freshwater fish northern Mexican gartersnake. This below and summarized in Table 1 species that are documented prey sampling effort in Mexico below. species for the northern Mexican geographically constitutes a small Table 1—Summary of northern gartersnake from areas within its portion of the range of the northern Mexican gartersnake status and threats historical distribution in Mexico. From Mexican gartersnake in that country, but by population in the United States. the status of those communities or fish it provides limited regional insight into (Note: ‘‘Extirpated’’ means that there species, we inferred a similar status for the species’ status. Population trends at have been no northern Mexican the northern Mexican gartersnake as we locations visited cannot be assessed gartersnakes reported for a decade or have no reason to conclude these because these sites have only been longer at a site within the historical particular predator-prey relationships visited once. distribution of the species, despite respond any differently to biological A research biologist with the survey efforts, and there is no community-level perturbations in Universidad Autonoma del Estado de expectation of natural recovery at the Mexico as has been observed reliably in Me´xico, who has been doing field the United States. See Factors A and C research on Mexican gartersnakes in site due to the presence of known or for analysis of threats to the habitat and central Mexico (within the distribution strongly suspected causes of extirpation. prey base. of northern Mexican gartersnakes) for ‘‘Extant’’ means areas where the species A large number of springs have dried approximately two decades, has is expected to reliably occur in up in several Mexican states within the documented the decline or appropriate habitat as supported by distribution of the northern Mexican disappearance of populations from museum records or recent, reliable gartersnake, particularly from the years drying of water bodies, water observations. ‘‘Unknown’’ means areas 1974–1994 in states including contamination, and other human where the species is known to have Chihuahua, Durango, Coahila, and San impacts where, 20 years ago, the species occurred based on museum records Luis Potosı´ (Contreras Balderas and was abundant (Manjarrez 2008). (mostly historical) but access is Lozano 1994, p. 381). Because this has Determining the status of the northern restricted, or survey data is unavailable eliminated the habitat and aquatic prey Mexican gartersnake in Mexico is or insufficient, or where threats could base of the snake, we conclude that the hampered by the lack of large-scale preclude occupancy.)
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Population locality Current status Regional historical or current threats
Gila River (outside of Highway 180 Extirpated ...... Factor A: Improper grazing, recreation, development, groundwater pumping, crossing) (Arizona, New Mexico). water diversions, channelization, dewatering, road construction/use, wildfire, intentional harm, dams. Factor C: Nonnative species, prey base reduction. Gila and San Francisco Headwaters Extirpated ...... Factor A: Improper grazing, recreation. (New Mexico). Factor C: Nonnative species, prey base reduction. Lower Colorado River from Davis Dam to Extirpated ...... Factor A: Recreation, development, road construction and use, borderland se- International Border (Arizona). curity and undocumented immigration, intentional harm, dams. Factor C: Nonnative species, prey base reduction. San Pedro River in United States (Ari- Extirpated ...... Factor A: Improper grazing, groundwater pumping, road construction and use, zona). borderland security and undocumented immigration, intentional harm. Factor C: Nonnative species, prey base reduction. Santa Cruz River downstream of the Extirpated ...... Factor A: Improper grazing, development, groundwater pumping, water diver- Nogales area of the International Bor- sions, channelization, road construction and use, borderland security and un- der (Arizona). documented immigration, intentional harm, contaminants. Factor C: Nonnative species, prey base reduction. Salt River (Arizona) ...... Extirpated ...... Factor A: Improper grazing, recreation, development, water diversions, wildfire, channelization, road construction/use, intentional harm, dams. Factor C: Nonnative species, prey base reduction. Rio San Bernardino from International Extirpated ...... Factor A: Borderland security and undocumented immigration, intentional Border to headwaters at Astin Spring harm. (San Bernardino National Wildlife Ref- Factor C: Nonnative species, prey base reduction. uge, Arizona). Factor E: Competition with Marcy’s checkered gartersnake. Agua Fria River (Arizona) ...... Extirpated ...... Factor A: Improper grazing, development, recreation, dams, road construction and use, wildfire, intentional harm. Factor C: Nonnative species, prey base reduction. Verde River upstream of Clarkdale (Ari- Extirpated ...... Factor A: Improper grazing, recreation, development, groundwater pumping, zona). water diversions, channelization, road construction and use, intentional harm. Factor C: Nonnative species, prey base reduction. Verde River from the confluence with the Extirpated ...... Factor A: Improper grazing, recreation, groundwater pumping, water diver- Salt upstream to Fossil Creek (Ari- sions, channelization, road construction and use, wildfire, development, in- zona). tentional harm, dams. Factor C: Nonnative species, prey base reduction. Potrero Canyon/Springs (Arizona) ...... Extirpated ...... Factor A: Improper grazing. Factor C: Nonnative species, prey base reduction. Tanque Verde Creek in Tucson (Arizona) Extirpated ...... Factor A: Improper grazing, recreation, development, groundwater pumping, road construction and use, intentional harm. Factor C: Nonnative species, prey base reduction. Rillito Creek in Tucson (Arizona) ...... Extirpated ...... Factor A: Improper grazing, recreation, development, groundwater pumping, road construction and use, intentional harm. Factor C: Nonnative species, prey base reduction. Agua Caliente Spring in Tucson (Ari- Extirpated ...... Factor A: Improper grazing, recreation, development, groundwater pumping, zona). road construction and use, intentional harm. Factor C: Nonnative species, prey base reduction. Babocamari Cienega (Arizona) ...... Extirpated ...... Factor A: Improper grazing. Factor C: Nonnative species, prey base reduction. Barchas Ranch, Huachuca Mountain Extirpated ...... Factor A: Improper grazing, borderland security and undocumented immigra- bajada (Arizona). tion, intentional harm. Factor C: Nonnative species, prey base reduction. Parker Canyon Lake and tributaries in Extirpated ...... Factor A: Improper grazing, recreation, road construction and use, borderland the Canelo Hills (Arizona). security and undocumented immigration, intentional harm, dams. Factor C: Nonnative species, prey base reduction. Oak Creek at Midgley Bridge (Arizona) ... Extirpated ...... Factor A: Improper grazing, recreation, development, intentional harm. Factor C: Nonnative species, prey base reduction. Santa Cruz River/Lower San Rafael Val- Extant ...... Factor A: Improper grazing, borderland security and undocumented immigra- ley (headwaters downstream to Inter- tion, intentional harm. national Border) (Arizona). Factor C: Nonnative species, prey base reduction. Verde River from the confluence with Extant ...... Factor A: Improper grazing, recreation, development, groundwater pumping, Fossil Creek upstream to Clarkdale water diversions, channelization, road construction and use, intentional (Arizona). harm, dams. Factor C: Nonnative species, prey base reduction. Oak Creek at Page Springs (Arizona) ..... Extant ...... Factor A: Development, construction, vehicle mortality. Factor C: Nonnative species, prey base reduction, domestic cat predation, parasites. Tonto Creek from mouth of Houston Extant ...... Factor A: Improper grazing, recreation, development, water diversions, chan- Creek downstream to Roosevelt Lake nelization, road construction and use, wildfire, intentional harm, dams, flood (Arizona). control. Factor C: Nonnative species, prey base reduction. Cienega Creek from headwaters down- Extant ...... Factor A: Improper grazing. stream to the ‘‘Narrows’’ just down- Factor C: Nonnative species, prey base reduction. stream of Apache Canyon (Arizona).
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Population locality Current status Regional historical or current threats
Pantano Wash (Cienega Creek) from Extant ...... Factor A: Improper grazing, development, wildfire. Pantano downstream to Vail (Arizona). Factor C: Nonnative species, prey base reduction. Appleton-Whittell Research Ranch and Extant ...... Factor A: Improper grazing. vicinity near Elgin (Arizona). Factor C: Nonnative species, prey base reduction. Upper Scotia Canyon in the Huachuca Unknown ...... Factor A: Wildfire. Mountains (Arizona). Factor C: Nonnative species, prey base reduction. Downstream portion of the Black River Unknown ...... Factor A: Improper grazing, recreation, intentional harm. drainage from the Paddy Creek con- Factor C: Nonnative species, prey base reduction. fluence (Arizona). Downstream portion of the White River Unknown ...... Factor A: Improper grazing, recreation, road construction and use, intentional drainage from the confluence of the harm. East/North (Arizona). Factor C: Nonnative species, prey base reduction. Big Bonito Creek (Arizona) ...... Unknown ...... Factor A: Improper grazing. Factor C: Nonnative species, prey base reductions. Lake O’ Woods (Lakeside, Arizona) ...... Unknown ...... Factor A: recreation, development, road construction/use, intentional harm. Factor C: Nonnative species, prey base reduction. Spring Creek above confluence with Oak Unknown ...... Factor A: Development. Creek (Arizona). Factor C: Nonnative species, prey base reduction. Bog Hole Wildlife Area (Arizona) ...... Unknown ...... Factor C: Nonnative species, prey base reduction. Upper 13 Tank, Patagonia Mountains Unknown ...... Factor A: Improper grazing. bajada (Arizona). Factor C: Nonnative species, prey base reduction. Babocamari River (Arizona) ...... Unknown ...... Factor A: Improper grazing. Factor C: Nonnative species, prey base reduction. Arivaca Cienega (Arizona) ...... Unknown ...... Factor A: Improper grazing, borderland security and undocumented immigra- tion, intentional harm. Factor C: Nonnative species, prey base reduction. Gila River at Highway 180 (New Mexico) Unknown ...... Factor A: Improper grazing, recreation, development, groundwater pumping, water diversions, channelization, dewatering, road construction/use, wildfire, intentional harm, dams. Factor C: Nonnative species, prey base reduction.
References: For each of the population northern Mexican gartersnake in the Girmendock and Young 1997, pp. 45– localities discussed in Table 1, a United States are also likely present in 52; Rinne et al. 1998, pp. 7–11; Belsky detailed textual discussion of the Mexico, as further discussed below, et al. 1999, pp. 8–12; Esque and identified threats, including applicable despite the lack of formal Schwalbe 2002, pp. 165, 190; Hancock reference citations, is found in documentation. Thus, we expect 2002, p. 765; Voeltz 2002, pp. 87–88; subsequent sections of this finding impacts to the habitat and the species to Webb and Leake 2005, pp. 305–308; related to each of the five listing factors. be similar in the United States and Holycross et al. 2006, pp. 52–61; Site-specific information from locations Mexico. McKinnon 2006a, 2006b, 2006c, 2006d, in Mexico is limited and, therefore, A. The Present or Threatened 2006e; Paradzick et al. 2006, pp. 88–93; locations in Mexico are not included in Destruction, Modification, or Segee and Neeley 1996, Executive this table. Where available, the Curtailment of Its Habitat or Range Summary, pp. 10–12, 21–23; Burger information from Mexico is presented 2008, USFS 2008; USFWS 2007, pp. 25, and cited in our discussion of the five Various threats that have affected and 35–39; Gila County Board of listing factors below. continue to affect riparian and aquatic Supervisors 2008, pp. 1–2; Kimmel In the discussions of Factors A communities that provide habitat for the 2008; Trammell 2008; Sanchez 2008; through E below, we describe the northern Mexican garter snake include Lyons and Navarro-Perez 1990, p. 37; known factors that have contributed to dams, water diversions, groundwater Minckley et al. 2002, pp. 696; Nijhuis the current status of the northern pumping, introduction of nonnative 2007, pp. 1–7; Ouren et al. 2007, pp. 16– Mexican gartersnake. For populations species (vertebrates, plants, and 22; Rorabaugh 2008, pp. 25–26). Threats within the United States, our analysis crayfish), woodcutting, recreation, to northern Mexican gartersnake habitat benefitted from the availability of mining, contaminants, urban and in Mexico include the intentional and specific research, monitoring, and other agricultural development, road unintentional introductions of studies. The discussion of these factors construction, improper livestock nonnative species, improper livestock that pertain to the status and threats to grazing, wildfires, and undocumented grazing, urbanization and development, the northern Mexican gartersnake in immigration (Hendrickson and water diversions and groundwater Mexico are mainly regional, or Minckley 1984, p. 161; Ohmart et al. pumping, loss of vegetation cover and statewide, in scope because, in many 1988, p. 150; Bahre 1995, pp. 240–252; deforestation, erosion, and pollution, as cases, there was limited specific Medina 1990, p. 351; Sullivan and well as impoundments and dams that information available. In some Richardson 1993, pp. 35–42; Fleischner have modified or destroyed riparian and instances, we do include discussion on 1994, pp. 630–631; Hadley and aquatic communities within Mexico in more refined geographic areas of Mexico Sheridan 1995; Hale et al. 1995, pp. areas where the species occurred when supported by the literature. It is 138–140; DeBano and Neary 1996, pp. historically (Conant 1974, p. 471; Lyons important to understand, however, that 73–75; Rinne and Neary 1996, p. 135; and Navarro-Perez 1990, p. 37; many of the threats that affect the Stromberg et al. 1996, pp. 124–127; Contreras Balderas and Lozano 1994, p.
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384; va Landa et al. 1997, p. 316; threats have been identified in the Many sub-basins, where cienegas Jime´nez-Ruiz et al. 2002, p. 458; decline of many native riparian flora have been severely modified or lost Minckley et al. 2002, pp. 696; Miller et and fauna species through habitat entirely, wholly or partially overlap the al. 2005, pp. 60–61; Abarca 2006; Burger modification and destruction, as well as historical distribution of the northern 2008; Luja and Rodrı´guez-Estrella 2008, nonnative species introductions. Mexican gartersnake, including the San pp. 17–22; Rorabaugh 2008, pp. 25–26; Researchers agree that the period from Simon, Sulphur Springs, San Pedro, and Manjarrez 2008). 1850 to 1940 marked the greatest loss Santa Cruz valleys of southeastern and Rorabaugh (2008, pp. 25–26) noted and degradation of riparian and aquatic south-central Arizona. The San Simon threats to northern Mexican communities in Arizona, which were Valley in Arizona possessed several gartersnakes and their native amphibian caused by anthropogenic (human- natural cienegas with luxuriant prey base in Sonora, which included caused) land uses and the primary and vegetation prior to 1885, and was used disease, pollution, improper livestock secondary effects of those uses as a watering stop for pioneers, military, grazing, conversion of land for (Stromberg et al. 1996, p. 114; Webb and and surveying expeditions (Hendrickson agriculture, nonnative plant invasions, Leake 2005, pp. 305–310). Many of and Minckley 1984, pp. 139–140). In the and logging. Ramirez Bautista and these land activities continue today and subsequent decades, the disappearance Arizmendi (2004, p. 3) stated that the are discussed in detail below. An of grasses and commencement of severe principal threats to northern Mexican estimated one-third of Arizona’s pre- erosion were the result of heavy grazing gartersnake habitat in Mexico include settlement wetlands have dried or have pressure by large herds of cattle, as well the drying of wetlands, improper been rendered ecologically as the effects from wagon trails that livestock grazing, deforestation, dysfunctional (Yuhas 1996). paralleled arroyos, occasionally crossed wildfires, and urbanization. In addition, Modification and Loss of Cienegas. them, and often required stream bank nonnative species, such as bullfrogs and Cienegas are particularly important modification (Hendrickson and sport and bait fish, have been habitat for the northern Mexican Minckley 1984, p. 140). Today, only the introduced throughout Mexico and gartersnake and are considered ideal for artificially maintained San Simon continue to disperse naturally, the species (Rosen and Schwalbe 1988, Cienega exists in this valley. Similar broadening their distributions (Conant p. 14). Hendrickson and Minckley accounts of past conditions, adverse 1974, pp. 487–489; Miller et al. 2005, (1984, p. 131) defined cienegas as ‘‘mid- effects from historical anthropogenic ´ pp. 60–61; Luja and Rodrıguez-Estrella elevation (3,281–6,562 ft (1,000–2000 activities, and subsequent reduction in 2008, pp. 17–22). m)) wetlands characterized by the extent and quality of cienega The activities outlined above for both permanently saturated, highly organic, habitats in the remaining valleys are the United States and Mexico and their reducing [lowering of oxygen level] also provided in Hendrickson and effects on the northern Mexican soils.’’ Many of these unique Minckley (1984, pp. 138–160). gartersnake are discussed in further Urban and Rural Development. communities of the southwestern detail below. It is important to recognize Development within and adjacent to United States, Arizona in particular, and that in most areas where northern riparian areas has proven to be a Mexico have been lost in the past Mexican gartersnakes historically or significant threat to riparian biological century to streambed modification, currently occur, two or more threats communities and their suitability for improper livestock grazing, may be acting in combination in their native species (Medina 1990, p. 351). influence on the suitability of those woodcutting, artificial drainage Riparian communities are sensitive to habitats or on the northern Mexican structures, stream flow stabilization by even low levels (less than 10 percent) of gartersnake itself. In our assessment of upstream dams, channelization, and urban development within a watershed the status of these habitats, discussion stream flow reduction from groundwater (Wheeler et al. 2005, p. 142). of the role that nonnative species pumping and water diversions Development along or within proximity introductions have had on habitat (Hendrickson and Minckley 1984, p. to riparian zones can alter the nature of suitability is critical. However, we 161). Stromberg et al. (1996, p. 114) stream flow dramatically, changing provide that discussion under ‘‘Factor state that cienegas were formerly once-perennial streams into ephemeral C. Disease and Predation’’ due to the extensive along streams of the streams, which has direct consequences intricate and complex relationship Southwest; however, most were on the riparian community (Medina nonnative species have with respect to destroyed during the late 1800s, when 1990, pp. 358–359) and, within direct and indirect pressures applied to groundwater tables declined several occupied habitat, the northern Mexican the northern Mexican gartersnake and to meters and stream channels became gartersnake. Medina (1990, pp. 358–359) its native prey base. incised. concluded that perennial streams had Nonnative shrub species in the genus greater tree densities in all diameter size Destruction and Modification of Tamarix, such as salt cedar, have been classes of Alnus oblongifolius (Arizona Riparian and Aquatic Biological widely introduced throughout the alder) and Acer negundo (box elder) as Communities western States and appear to thrive in compared to ephemeral reaches where The modification and destruction of regulated river systems (Stromberg and small-diameter trees were absent. Small- aquatic and riparian communities in the Chew 2002, pp. 210–213). Tamarix diameter trees assist the northern post-settlement arid southwestern invasions may result in habitat Mexican gartersnake by providing United States is well documented alteration from potential effects to water additional habitat complexity and cover (Medina 1990, p. 351; Sullivan and tables, changes to canopy and ground needed to reduce predation risk and Richardson 1993, pp. 35–42; Fleischner vegetation structures, and increased fire enhance the usefulness of areas for 1994, pp. 630–631; Stromberg et al. risk, which hasten the loss of native maintaining optimal body temperature. 1996, pp. 113, 123–128; Girmendock cottonwood and willow communities Obvious examples of the influence of and Young 1997, pp. 45–52; Belsky et and affect the suitability of the urbanization and development can be al. 1999, pp. 8–12; Webb and Leake vegetation component to northern observed within the areas of greater 2005, pp. 305–310; Holycross et al. Mexican gartersnake habitat (Stromberg Tucson and Phoenix, Arizona, where 2006, pp. 52–61; Nijhuis 2007, pp. 1–7; and Chew 2002, pp. 211–212; USFWS impacts have modified riparian Ouren et al. 2007, pp. 16–22). Several 2002b, p. H–9). vegetation, structurally altered stream
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channels, facilitated nonnative species These projects may adversely affect the Medina (1990, p. 351) points out that introductions, and dewatered large northern Mexican gartersnake directly many real estate investors are looking reaches of formerly perennial rivers through physical harm or injury or for aesthetically scenic, mild climes to where the northern Mexican gartersnake indirectly from effects to its habitat or enjoy seasonally or year-round and historically occurred (Santa Cruz, Gila, prey base. hence choose to develop pre- or post- and Salt rivers, respectively). The Bubbling Ponds hatchery, which retirement properties that are within or Urbanization and development of these raises nonnative and native fish adjacent to riparian areas due to their areas, along with the introduction of (largemouth bass, smallmouth bass, and aesthetic appeal and available water, nonnative species, are largely bluegill, Colorado River pikeminnow, especially in the southwestern United responsible for the likely extirpation of razorback sucker), is located on Oak States. Arizona increased its population the northern Mexican gartersnake from Creek, just north of the Page Springs by 394 percent from 1960 to 2000, and these areas. hatchery, and comprises 2 parcels is second only to Nevada as the fastest Urbanization on smaller scales can approximately 117 ac (47 ha) in size growing State in terms of human also impact habitat suitability and the (AGFD 1997b, p. 2). The hatchery population (Social Science Data prey base for the northern Mexican consists of 11 earthen ponds and 6 lined Analysis Network (SSDAR) 2000, p.1). gartersnake. Regional development and ponds totaling 10 surface acres (4 Over the same time period, population subsequent land use changes, spurred surface hectares), 3 residential growth rates in Arizona counties where by increasing populations, along lower structures, and the hatchery building the northern Mexican gartersnake Tonto Creek and within the Verde (AGFD 1997b, p. 2). Hatchery operations historically occurred or may still occur Valley where northern Mexican are confined to 17 of the 117 ac (7 of 47 have varied by county but are no less gartersnakes occur, continue to threaten ha) and have been modified extensively remarkable, and all are increasing: this snake’s habitat and affect the (AGFD 1997b, p. 4). The remaining 100 Maricopa (463 percent); Pima (318 habitat’s suitability for the northern ac (40 ha) support riparian woodland percent); Santa Cruz (355 percent); Mexican gartersnake and its prey and forest along Oak Creek (AGFD Cochise (214 percent); Yavapai (579 species (Girmendock and Young 1997, 1997b, p. 4). Northern Mexican percent); Gila (199 percent); Graham pp. 45–52; Voeltz 2002, pp. 58–59, 69– gartersnakes are presumed to occur (238 percent); Apache (228 percent); 71; Paradzick et al. 2006, pp. 89–90). throughout this property; using the Navajo (257 percent); Yuma (346 Holycross et al. (2006, pp. 53, 56) earthen ponds for foraging on young percent); LaPaz (142 percent); and recently documented the damage and bullfrogs, their tadpoles, and fish, and Mohave (2004 percent) (SSDAR 2000). removal of northern Mexican using areas near or adjacent to Population growth trends in Arizona, gartersnake streamside habitat from structures on the property. Current and Maricopa County in particular, are development in the vicinity of Rock future management and maintenance of expected to continue into the future. Springs along the Agua Fria River and Bubbling Ponds include a variety of The Phoenix metropolitan area, founded also within the Verde Valley along the activities that would potentially affect in part due to its location at the junction Verde River. snake habitat, such as the maintenance of the Salt and Gila rivers, is a Ongoing small-scale development of roads, buildings, fences, equipment, population center of 3.63 million projects within the Page Springs and as well as development (residences, people. The Phoenix metropolitan area Bubbling Ponds fish hatcheries along storage facilities, asphalt, resurfacing, is the sixth largest in the United States Oak Creek, upstream of its confluence etc.) and both human- and habitat-based and resides in the fastest growing with the Verde River, occur within enhancement projects (AGFD 1997b, pp. county in the United States since the potentially the most robust remaining 8–9; Wilson and Company 1991, pp. 1– 2000 census (Arizona Republic 2006). population of northern Mexican 40; 1992, pp. 1–99). Implementation of Given the large amount of perennial gartersnakes in the United States (AGFD such projects is expected to result in the habitat at the confluence of two large, 1997a, pp. 1–13; 1997b, pp. 1–12). The damage or removal of habitat or flowing rivers that was historically Page Springs trout hatchery is an 82- potentially the contamination of habitat present in this area prior to settlement, acre (ac) (33-hectare (ha)) facility from the use of industrial products and northern Mexican gartersnakes likely located within a semi-desert grassland chemicals. The small-scale development maintained dense populations in this vegetative community (AGFD 1997a, p. projects at these hatcheries may injure region of Arizona. However, with the 3). It is the largest State-run hatchery or kill northern Mexican gartersnakes or burgeoning population growth and and was renovated in 1993, resulting in their prey base, and may also associated urbanization and construction-related impacts such as the temporarily damage or remove occupied development that have occurred since, removal of riparian vegetation and other habitat. The Arizona Game and Fish any remaining habitat for the northern earth-moving activities to occupied Department is a long-standing partner in Mexican gartersnake has been rendered snake habitat (AGFD 1997a, p.1). research and survey efforts related to the unsuitable and the subspecies is now Current and future management and northern Mexican gartersnake, and there likely extirpated from this area and its maintenance of Page Springs include a is an ongoing population study at the recovery is unlikely. variety of activities that would hatcheries. Adaptive management in Massive growth predictions have been potentially affect occupied snake relation to activities at the hatcheries, as made for traditionally rural portions of habitat, such as the maintenance of informed by the population study, will Arizona. The populations of developing roads, buildings, fences, equipment, as help reduce the overall effects to cities and towns of the Verde watershed well as development (residences, gartersnakes and their habitat at the are expected to more than double in the storage facilities, asphalt, resurfacing, hatcheries. next 50 years, which may pose etc.) and both human- and habitat-based The effects of urban and rural exceptional threats to riparian and enhancement projects (AGFD 1997a, p. development are expected to increase as aquatic communities of the Verde 8). Implementation of such projects is human populations increase. Consumer Valley where northern Mexican expected to result in the damage or interest in second home and/or gartersnakes occur (Girmendock and removal of habitat or potentially the retirement real estate investments has Young 1993, p. 47; American Rivers contamination of habitat from the use of increased significantly in recent times 2006; Paradzick et al. 2006, p. 89). industrial products and chemicals. within the southwestern United States. Communities in Yavapai and Gila
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counties such as the Prescott-Chino infrastructure. The threats to northern pollutants (Waters 1995, p. 42; Wheeler Valley, Strawberry, Pine, and Payson Mexican gartersnake habitat in riparian et al. 2005, pp. 145, 148–149). Sediment have all seen rapid population growth and aquatic communities in Mexico can adversely affect fish populations in recent years. For example, the vary in their significance, based on used as prey by the northern Mexican population in the town of Chino Valley, geographical distribution of land gartersnake by (1) interfering with at the headwaters of the Verde River, management activities and urban respiration; (2) reducing the has grown by 22 percent between 2000 centers, but are expected to continue effectiveness of fish’s visually-based and 2004; Gila County, which includes into the future. hunting behaviors; and (3) filling in reaches of the Salt, White, and Black Mexico’s human population grew 700 interstitial spaces of the substrate, rivers and Tonto Creek, grew by 20 percent from 1910 to 2000 (Miller et al. which reduces reproduction and percent between 2000 and 2003 2005, p. 60). Mexico’s population foraging success of fish (Wheeler et al. (http://www.census.gov). The upper San increased by 245 percent from 1950 to 2005, p. 145). Excessive sediment also Pedro River is also the location of rapid 2002, and is projected to grow by fills in intermittent pools required for population growth in the Sierra Vista- another 28 percent by 2025 amphibian prey reproduction and Huachuca City-Tombstone-Benson area (EarthTrends 2005). As of 1992, Mexico foraging. Fine sediment pollution in (http://www.census.gov). All of these had the second highest gross domestic streams impacted by highway communities are near or within the product in Latin America at 5.8 percent, construction without the use of vicinity of historical or current northern following Brazil (DeGregorio 1992, p. sediment control structures was 5 to 12 Mexican gartersnake populations. 60). As a result of NAFTA, the number times greater than control streams In Mexico, the magnitude and of maquiladoras (export assembly (Wheeler et al. 2005, p. 144). As stated significance of adverse effects to plants) is expected to increase by as above, sediment can lead to several riparian communities related to many as 3,000 to 4,000 (Contreras effects in resident fish species used by development lags somewhat behind that Balderas and Lozano 1994, p. 384). To northern Mexican gartersnakes as prey, experienced in the United States due to accommodate Mexico’s increasing which can ultimately cause increased slower population and economic human population, rural areas are direct mortality, reduced reproductive growth, but it is reported that threats to largely devoted to food production success, lower overall abundance of the riparian and aquatic communities that based on traditional methods, which has northern Mexican gartersnake, lower have been observed in Arizona are led to serious losses in vegetative cover species diversity of prey, and reductions currently occurring with increasing and soil erosion (va Landa et al. 1997, in food base as documented by Wheeler significance in Mexico (Conant 1974, p. 316). et al. (2005, p. 145). The underwater pp. 471, 487–489; Contreras Balderas Road Construction, Use, and foraging ability of northern Mexican and Lozano 1994, pp. 379–381; va Maintenance. Roads cover gartersnakes is also directly approximately 1 percent of the land area Landa et al. 1997, p. 316; Miller et al. compromised by excessive turbidity in the United States, but negatively 2005, p. 60–61; Abarca 2006; Rosen caused by sedimentation of water affect 20 percent of the habitat and biota 2006). bodies, because this snake locates its Ortega-Huerta and Kral (2007, p. 1) in the United States (Angermeier et al. prey visually. found that land legislation within 2004, p. 19). Roads pose unique threats Mexico has changed considerably over to herpetofauna and specifically to Metal contaminants, including iron, recent years to integrate free market species like the northern Mexican zinc, lead, cadmium, nickel, copper, policies into local agricultural gartersnake, its prey base, and the and chromium, are associated with production methods that may result in habitat where it occurs through: (1) highway construction and use (Foreman the loss of land management practices Fragmentation, modification, and and Alexander 1998, p. 220; Hopkins et that protect the natural environment. destruction of habitat; (2) increase in al. 1999, p. 1260; Campbell et al. 2005, Community-based lands generally genetic isolation; (3) alteration of p. 241; Wheeler et al. 2005, pp. 146– presented higher instance of habitat movement patterns and behaviors; (4) 149) and are bioaccumulative. A conservation in terms of natural facilitation of the spread of nonnative bioaccumulative substance increases in vegetation, higher species aggregations, species via human vectors; (5) an concentration in an organism or in the more evenly distributed cover types, increase in recreational access and the food chain over time. A mid- to higher- and greater species richness (Ortega- likelihood of subsequent, decentralized order predator, such as a gartersnake, Huerta and Kral 2007, p. 1). These urbanization; (6) interference with or may therefore accumulate these types of correlations between land ownership inhibition of reproduction; (7) contaminants over time in their fatty and bird and mammal species richness contributions of pollutants to riparian tissues, which may lead to adverse can be generally extrapolated to other and aquatic communities; and (8) health effects. Several studies have aspects of biotic communities, including population sinks (a factor resulting in addressed the effects of bioaccumulative the aquatic and semi-aquatic unnaturally high death rates that exceed substances on watersnakes. We find communities within areas. A shift away birth rates within a population) through these studies relevant because from traditional land management in direct mortality (Rosen and Lowe 1994, watersnakes and gartersnakes have very Mexico presents threats to riparian and pp. 146–148; Waters 1995, p. 42; Carr similar life histories and prey bases and, aquatic habitats occupied by the and Fahrig 2001, pp. 1074–1076; Hels therefore, the effects from northern Mexican gartersnake. and Buchwald 2001, p. 331; Smith and contamination of their habitat from Collectively, development impacts of Dodd 2003, pp. 134–138; Angermeier et bioaccumulative agents are expected to all types in Mexico are expected to al. 2004, pp. 19–24; Shine et al. 2004, be similar. Campbell et al. (2005, pp. continue as a result of Mexico’s pp. 9, 17–19; Andrews and Gibbons 241–243) found that metal expanding role as an economical labor 2005, pp. 777–781; Wheeler et al. 2005, concentrations accumulated in the force for international manufacturing pp. 145, 148–149; Roe et al. 2006, p. northern watersnake (Nerodia sipedon) under the North American Free Trade 161). at levels six times that of their primary Agreement (NAFTA) and the Construction and maintenance of food item, the central stoneroller (fish) subsequent increase in population size, roads and highways near riparian areas (Campostoma anomalum). Metals, in economic growth and development, and can be a source of sediment and trace amounts, affect the structure and
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function of the liver and kidneys of mortality rates due to roads are higher occupied habitat and may even lead to vertebrates and may also act as in vagile (mobile) species, such as depressed populations of snakes neurotoxins, affecting nervous system gartersnakes (active hunters), than those depending on the rate of use and function (Rainwater et al. 2005, p. 670). of more sedentary species, which more number of trails within a given area Metals may also be sequestered in the commonly employ sit-and-wait foraging (Ouren et al. 2007, pp. 20–21). This skin of reptiles, but this effect is strategies. Roads that bisect wetland threat may be even more extensive from tempered somewhat by ecdysis (the communities also act as mortality sinks OHVs than from conventional vehicles regular shedding or molting of the skin) in the dispersal or migratory movements because OHV trails often travel through (Burger 1999, p. 212). Hopkins et al. of snakes (Roe et al. 2006, p. 161). The undeveloped habitat and often cross (1999, p. 1261) found that metals may effect of road mortality of snakes directly through waterbodies. OHV use even interfere with metabolic rates of becomes most significant in the case of may also affect northern Mexican banded watersnakes (Nerodia fasciata), small, highly fragmented populations gartersnake habitat by reducing altering the allocation of energy between where the chance removal of mature vegetation cover and plant species maintenance and reproduction, females from the population may diversity, reducing infiltration rates, reducing the efficiency of energy stores, appreciably degrade the viability of a increasing erosion, and reducing habitat and forcing individuals to forage more population. connectivity (Ouren et al. 2007, pp. 6– often, which increases activity costs (the Even lightly used roads may also lead 7, 11, 16). energy expended in hunting, which to mortality of northern Mexican Roads create access to areas that were affects the net nutritional intake of an gartersnakes. For example, gravel roads previously visited only infrequently or organism) and predation risk. that surround the hatchery ponds that were inaccessible to humans, increasing are traveled by hatchery, research lab, the frequency and significance of Snakes of all species are particularly and resident vehicles at the Bubbling anthropogenic threats to riparian areas vulnerable to mortality when they Ponds fish hatchery have resulted in and fragmenting the landscape, which attempt to cross roads. Snakes are four documented northern Mexican in addition to direct effects to snakes animals that derive heat from warm gartersnake mortalities since mortality and habitat, may genetically isolate surfaces, which often compels them to data began being collected in 2006 herpetofaunal populations (Rosen and slow down or even stop and rest on road (Boyarski 2008a, pp. 1–4). These vehicle Lowe 1994, pp. 146–148; Andrews and surfaces that have been warmed by the mortalities represent 50 percent of the Gibbons 2005, p. 772). sun as they attempt to cross (Rosen and mortalities documented at the McCranie and Wilson (1987, p. 2) Lowe 1994, p. 143). Gartersnakes are hatcheries. Of note is the fact that these discuss threats to the pine-oak generally diurnal (active during daylight vehicles are likely traveling at slow communities of higher elevation hours) and are often active when traffic speeds, which indicates that even slow- habitats within the distribution of the densities are greatest (Rosen and Lowe moving vehicles pose a hazard to northern Mexican gartersnake in the 1994, p. 147). Mortality data have been crossing and basking snakes. Wallace et Sierra Madre Occidental in Mexico, collected at the Bubbling Ponds al. (2008, pp. 243–244) documented a specifically noting that ‘‘* * * the Hatchery since 2006. Of the eight dead vehicle-related mortality of a northern relative pristine character of the pine- specimens, half were struck by vehicles Mexican gartersnake on Arizona State oak woodlands is threatened * * * on roads adjacent to the hatchery ponds Route 188 near Tonto Creek that every time a new road is bulldozed up that are crossed by northern Mexican occurred in 1995. As shown in the the slopes in search of new madera or gartersnakes in traveling between ponds above examples, vehicle-related pasturage. Once the road is built, further to forage (Boyarski 2008a). Van mortalities of northern Mexican development follows; pueblos begin to Devender and Lowe (1977, p. 47), gartersnakes likely occur routinely along pop up along its length * * *.’’ Several however, observed several northern roads or trails adjacent to occupied drainages that possess suitable habitat Mexican gartersnakes crossing the road habitat throughout the range of the for the species occur in the area at night after the commencement of the subspecies but are generally difficult to referenced above by McCranie and summer monsoon (rainy season), which document. Wilson (1987, p. 2) including the Rio de highlights the seasonal variability in Off-highway vehicle (OHV) use has la Cuidad, Rio Quebrada El Salto, Rio surface activity of this snake. Perhaps grown considerably in Arizona. For Chico, Rio Las Bayas, Rio El Cigarrero, the most common factor in road example, as of 2007, 385,000 OHVs Rio Galindo, Rio Santa Barbara, and the mortality of snakes is the propensity for were registered in Arizona (a 350 Rio Chavaria. drivers to intentionally run over snakes, percent increase since 1998) and 1.7 While snakes of all species may suffer which generally make easy targets million people (29 percent of the direct mortality as a result of attempting because they usually cross roads at a Arizona’s public) engaged in off-road to cross roads, Andrews and Gibbons perpendicular angle (Klauber 1956, p. activity from 2005–2007 (Sacco 2007). (2005, pp. 777–779) found that many 1026; Langley et al. 1989, p. 47; Shine Over half of OHV users reported that individuals of small, diurnal snake et al. 2004, p. 11). This driving behavior merely driving off-road was their species avoid open areas (e.g., roads) is exacerbated by the general animosity primary activity, versus using the OHV instinctively in order to lower predation that humans have toward snakes (Ernst for the purpose of hunting, fishing, or rates, which represents a different type and Zug 1996, p. 75; Green 1997 pp. hiking (Sacco 2007). Given the of threat from roads. Shine et al. (2004, 285–286). In fact, Langley et al. (1989, pervasive use of OHV’s on the p. 9) found that the common gartersnake p. 47) conducted an experiment on the landscape, OHV-related mortalities are typically changed direction when propensity for drivers to hit reptiles on likely a threat to northern Mexican encountering a road. These avoidance the road using turtle and snake models gartersnakes. Ouren et al. (2007, pp. 16– behaviors by individuals aversive to and found that many people have a 22) provide additional data on the crossing roads affect movement patterns greater desire to hit a snake on the road effects of OHV use on wildlife. and may ultimately affect reproductive than any other animal; several drivers Specifically, OHV use may cause output within populations (Shine et al. actually stopped and backed-over the mortality or injury to species, such as 2004, pp. 9, 17–19). Not crossing roads snake mimic to ensure it was dead. Roe northern Mexican gartersnakes, that can reduce the amount of habitat et al. (2006, p. 161) conclude that attempt to cross trails created through available for individual snakes to find
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prey, mates, etc. This avoidance located near urban areas are vulnerable can follow. This situation has been behavior has been observed in the to the effects of increased recreation created by groundwater use by the common gartersnake (Thamnophis with predictable changes in the type community of Sierra Vista in Cochise sirtalis), a sister taxon to the Mexican and intensity of land use following County, which continues to threaten the gartersnake with similar life histories residential development. An example of riparian community along the upper and behavior (Shine et al. 2004, p. 9). such an area within the existing San Pedro River where the northern In our discussion and as evidenced by distribution of the northern Mexican Mexican gartersnake historically the literature we reviewed on the effect gartersnake is the Verde Valley. The occurred. Continued groundwater of roads on snake movements, we reach of the Verde River that winds pumping at such levels draws down the acknowledge the individuality of snakes through the Verde Valley receives a high aquifer sufficiently to create a water- in their behaviors towards road amount of recreational use from people level gradient away from the stream and crossings. living in central Arizona (Paradzick et floodplain (Webb and Leake 2005, p. In addition to altering the movement al. 2006, pp. 107–108). Increased human 309). Finally, complete disconnection of patterns of some snakes, roads interfere use results in the trampling of near- the aquifer and the stream results in with the male gartersnake’s olfactory- shore vegetation, which reduces cover strong negative effects to riparian driven ability to follow the pheromone for gartersnakes, especially newborns. vegetation (Webb and Leake 2005, p. trails left by receptive females (Shine et Increased human visitation in occupied 309). If complete disconnection occurs, al. 2004, pp. 17–18). This effect to the habitat also increases the potential for the hyporheic zone could be adversely male’s ability to efficiently trail females human-gartersnake interactions, which affected. The hyporheic zone can may exacerbate the effects of low frequently leads to the capture, injury, promote ‘‘hot spots’’ of productivity population density and fragmentation or death of the snake (Rosen and where groundwater upwelling produces that affect several species of snakes, Schwalbe 1988, p. 43; Ernst and Zug nitrates that can enhance the growth of including the northern Mexican 1996, p. 75; Green 1997, pp. 285–286; vegetation, but its significance is gartersnake. Because the male Nowak and Santana-Bendix 2002, p. contingent upon its activity and extent gartersnake’s ability to trail females is 39). Recreational activities in the of connection with the groundwater hampered by roads, the extra time and Southwest are often tied to water bodies (Boulton et al. 1998, p. 67; Boulton and distance traveled by male snakes and riparian areas. Increased Hancock 2006, pp. 135, 138). Such ‘‘hot seeking receptive females increases recreational impacts on the quantity and spots’’ can enhance the quality of exposure to predation and subsequently quality of water, as well as the adjacent northern Mexican gartersnake habitat. increases mortality rates (Shine et al. vegetation, are threats to local Conversely, changes to the duration and 2004, pp. 18–19). Although the northern populations of the northern Mexican timing of upwelling can potentially lead Mexican gartersnake was not the subject gartersnake. to localized extinctions in biota of the 2004 Shine et al. study, similar (Boulton and Hancock 2006, p. 139), Groundwater Pumping, Surface Water responses can be expected in the reducing gartersnake habitat suitability. northern Mexican gartersnake because Diversions, and Flood Control. The effects of groundwater pumping its life history is similar to the study’s Increased urbanization and population on surface water flow and riparian subject species (i.e., the common growth results in an increase in the communities have been observed in the gartersnake). demand for water and, therefore, water Santa Cruz, San Pedro, and Verde rivers Roads also affect prey availability for development projects. Collier et al. as a result of groundwater demands of northern Mexican garter snakes. Roads (1996, p. 16) mention that water Tucson, Sierra Vista, and the rapidly tend to adversely affect aquatic breeding development projects are one of two growing Prescott Valley, respectively anuran populations more so than other main causes of decline of native fish in (Stromberg et al. 1996, pp. 113, 124– species due to their activity patterns the Salt and Gila rivers of Arizona. 128; Rinne et al. 1998, p. 9; Voeltz 2002, (mass movements of individuals), Municipal water use in central Arizona pp. 45–47, 69–71). Along the upper San population structures (large cohorts of has increased by 39 percent in the last Pedro River, Stromberg et al. (1996, pp. similarly aged individuals within a 8 years (American Rivers 2006). Water 124–127) found that wetland population), and preferred habitats for development and urbanization is herbaceous species, important as cover which are often adjacent to roads and often supplied by groundwater pumping for northern Mexican gartersnakes, are usually constrained to aquatic or and surface water diversions from the most sensitive to the effects of a semiaquatic areas (Hels and Buchwald sources that include reservoirs and declining groundwater level. Webb and 2001, p. 331). Carr and Fahrig (2001, pp. Central Arizona Project’s allocations Leake (2005, pp. 302, 318–320) 1074–1076) found that populations of from the Colorado River. The hydrologic described a correlative trend regarding highly mobile anuran species such as connection between groundwater and vegetation along southwestern streams leopard frogs (Rana pipiens) were run surface flow of intermittent and from historically being dominated by over more frequently than more perennial streams is becoming better marshy grasslands preferable to sedentary species and that population understood. Groundwater pumping northern Mexican gartersnakes, to persistence can be at risk depending on creates a cone of depression within the currently being dominated by woody traffic densities, which may adversely affected aquifer that slowly radiates species more tolerant of declining water affect the prey base for northern outward from the well site. When the tables due to their associated deeper Mexican gartersnakes because leopard cone of depression intersects the rooting depths. frogs are a primary prey species. hyporheic zone of a stream (the active The full effects of large-scale Recreation. As discussed above, transition zone between two adjacent groundwater pumping associated with population growth trends are expected ecological communities under or beside the proposed Big Chino Water Ranch to continue into the future. Expanding a stream channel or floodplain between Project and its associated 30-mile (48- population growth leads to higher the surface water and groundwater that km), 36-in (91-cm) diameter pipeline recreational use of riparian areas, as contributes water to the stream itself), have yet to be realized in the Verde evidenced along reaches of the Salt and the surface water flow may decrease, River (McKinnon 2006c). This Verde rivers in proximity to the Phoenix and the subsequent drying of riparian groundwater pumping and inter-basin metropolitan area. Riparian areas and wetland vegetative communities transfer project is projected to deliver
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2.8 billion gallons of groundwater groundwater supply and an overdraft Trammell 2008). Mitigation measures annually from the Big Chino sub-basin has occurred. In these areas, that have been discussed include aquifer to the rapidly growing area of groundwater use has exceeded the rate removal of riparian vegetation, removal Prescott Valley for municipal use that precipitation can recharge the of debris piles, potential channelization (McKinnon 2006c). The Big Chino sub- aquifer, which leads to conditions of Tonto Creek, improvements to basin provides 86 percent of the described above. Geographically, all five existing flood control structures or baseflow to the upper Verde River AMAs overlap the historical addition of new structures, and the (American Rivers 2006; McKinnon distribution of the northern Mexican construction of new bridges. Adverse 2006a). The potential for this project to gartersnake in Arizona. The declaration effects of these types of activities to obtain funding and approval for of these AMAs further illustrates the aquatic and riparian habitat and to the implementation has placed the Verde condition and future threats to riparian northern Mexican gartersnake or its prey River on American River’s 2006 ‘‘Ten habitat in these areas and are a cause of species will result from the physical Most Endangered Rivers List’’ concern for the long-term maintenance alteration or destruction of habitat, (American Rivers 2006). This potential of historical and occupied northern significant increases to flow velocity, reduction or loss of baseflow in the Mexican gartersnake habitat. Such and removal of key foraging habitat and Verde River could seasonally dry up overdrafts reduce surface water flow of areas to hibernate, such as debris jams. large reaches or adversely affect the streams that are hydrologically Specifically, flood control projects riparian community and the suitability connected to the aquifer under stress, permanently alter stream flow of the habitat for remaining populations which can be further exacerbated by the characteristics and have the potential to of the northern Mexican gartersnake and surface water diversions. make the stream unsuitable as habitat its prey species in that area. To accommodate the needs of rapidly for the northern Mexican gartersnake by Within the Verde River watershed, growing rural and urban populations, reducing or eliminating stream sinuosity and particularly within the Verde Valley surface water is commonly diverted to and associated pool and backwater where the northern Mexican gartersnake serve many industrial and municipal habitats that are critical to northern is believed to currently remain, several uses. These water diversions have Mexican gartersnakes and their prey other activities continue to threaten dewatered large reaches of once species. Threats presented by these surface flows (Rinne et al. 1998, p. 9; perennial or intermittent streams, flood control planning efforts are Paradzick et al. 2006, pp. 104–110). The adversely affecting northern Mexican considered imminent. demands for surface water allocations gartersnake habitat throughout its range In Mexico, Conant (2003, p. 4) noted from rapidly growing communities and in Arizona and New Mexico. Many human-caused threats to seven agricultural and mining interests have tributaries of the Verde River are fragmented, highly localized subspecies altered flows or dewatered significant permanently or seasonally dewatered by of Mexican gartersnake in the reaches during the spring and summer water diversions for agriculture Transvolcanic Belt Region of southern months in some of the Verde River’s (Paradzick et al. 2006, pp. 104–110). Mexico, which extends from southern larger, formerly perennial tributaries Effects from flood control projects Jalisco eastward through the State of such as Wet Beaver Creek, West Clear threaten riparian and aquatic habitat, as Mexico to central Veracruz. Although Creek, and the East Verde River, which well as threaten the northern Mexican this is a relatively small area, rural land may have supported the northern gartersnake directly. Kimmell (2008), uses are widespread in the region and Mexican gartersnake (Girmendock and Gila County Board of Supervisors these threats can be extrapolated to Young 1993, pp. 45–47; Sullivan and (2008), Trammell (2008), and Sanchez other areas of that region within the Richardson 1993, pp. 38–39; Paradzick (2008) all discuss a growing concern of distribution of the northern Mexican et al. 2006, pp. 104–110). Groundwater residents that live within or adjacent to gartersnake in Mexico. Some of these pumping in the Tonto Creek drainage the floodplain of Tonto Creek in Gila threats included water diversions, regularly eliminates surface flows County, Arizona, both upstream and pollution (e.g., discharge of raw during parts of the year (Abarca and downstream of the town of Gisela, sewage), sedimentation of aquatic Weedman 1993, p. 2). The upper Gila Arizona. Specifically, there is growing habitats, and increased dissolved River is also threatened by water concern to address threats to private nutrients, resulting in decreased diversions and water allocations. In property and associated infrastructure dissolved oxygen, in still-water habitats. New Mexico, a proposed water project posed by flooding of Tonto Creek Conant (2003, p. 4) stated that many of that resulted from a landmark Gila River (Sanchez 2008). The only known these threats were evident during his water settlement in 2004 allows New remaining population of northern field work in the 1960s, but that they are Mexico the right to withhold 4.5 billion Mexican gartersnakes within the large ‘‘continuing with increased velocity.’’ gallons of surface water every year Salt River watershed occurs on Tonto Water pollution, dams, groundwater (McKinnon 2006d). If this proposed Creek. The status of the northern pumping, and impoundments were water diversion project is implemented, Mexican gartersnake on tribal lands identified by Miller et al. (2005, pp. 60– in dry years, currently perennial reaches within the Salt River watershed remains 61) as significant threats to aquatic biota of the upper Gila River will dry unknown. In Resolution No. 08–06–02, in Mexico. Miller et al. (2005, p. 60) completely, which removes all the Gila County Board of Supervisors stated that ‘‘During the time we have suitability of this habitat for the has proactively declared a state of collectively studied fishes in Me´xico northern Mexican gartersnakes and a emergency within Gila County as a and southwestern United States, the host of other riparian and aquatic result of the expectation for heavy rain entire biotas of long reaches of major species (McKinnon 2006d). and snowfall causing repetitive flooding streams where the northern Mexican The Arizona Department of Water conditions (Gila County Board of gartersnake is distributed, such as the Resources (ADWR) manages water Supervisors 2008). In response, the Rı´o Grande de Santiago below supplies in Arizona and has established Arizona Division of Emergency Guadalajara (Jalisco) and Rı´o Colorado five Active Management Areas (AMA) Management called meetings and (lower Colorado River in Mexico) across the State (ADWR 2006). An AMA initiated discussions among downstream of Hoover (Boulder) Dam is established by ADWR when an area’s stakeholders in an attempt to mitigate (in the United States), have simply been water demand has exceeded the these flooding concerns (Kimmell 2008, destroyed by pollution and river
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alteration.’’ Near Torreo´n, Coahuila, Chapala and its outlet to the Rı´o Grande Stromberg and Chew (2002, p. 198) and where the northern Mexican gartersnake de Santiago (major declines in Trimble and Mendel (1995, p. 243) also occurs, groundwater pumping has freshwater fish species, p. 106); discussed the propensity for poorly resulted in flow reversal, which has medium-sized streams throughout the managed cattle to remain within or dried up many local springs, drawn Sierra Madre Occidental (localized adjacent to riparian communities. arsenic-laden water to the surface, and extirpations, logging, dewatering, pp. Trimble and Mendel (1995, p. 243) resulted in adverse human health effects 109, 177, 247); the Rio Conchos stated that ‘‘Cows, unlike sheep, appear in that area. Severe water pollution from (extirpations of freshwater fish species, to love water and spend an inordinate untreated domestic waste is evident p. 112); the rı´os Casas Grandes, Santa amount of time together lounging in downstream of large Mexican cities, Marı´a, del Carmen, and Laguna streams and ponds, especially in such as Mexico City, and inorganic Bustillos (water diversions, groundwater summer (surface-active season for pollution from nearby industrialized pumping, channelization, flood control reptiles and amphibians), sometimes areas and agricultural irrigation return practices, pollution, and introduction of going in and coming out several times flow has dramatically affected aquatic nonnative species, pp. 124, 197); the Rı´o in the course of a day.’’ Expectedly, this communities through contamination Santa Cruz (extirpations, p. 140); the Rı´o behavior is more pronounced in more (Miller et al. 2005, p. 60). Miller et al. Yaqui (nonnative species, pp. 148, Plate arid regions (Trimble and Mendel 1995, (2005, p. 61) provides an excerpt from 61); the Rı´o Colorado (nonnative p. 243). In one rangeland study, it was Soto Galera et al. (1999) addressing the species, p. 153); the rı´os Fuerte and concluded that 81 percent of the threats to the Rı´o Lerma, Mexico’s Culiaca´n (logging, p. 177); canals, vegetation that was consumed, longest river, and which is occupied by ponds, lakes in the Valle de Me´xico trampled, or otherwise removed was the northern Mexican gartersnake: ‘‘The (nonnative species, extirpations, from a riparian area, which amounted to basin has experienced a staggering pollution, pp. 197, 281); the Rı´o Verde only 2 percent of the total grazing space amount of degradation during the 20th Basin (dewatering, nonnative species, (Trimble and Mendel 1995, p. 243). Century. By 1985–1993, over half of our extirpations, Plate 88); the Rı´o Mayo Another study reported that grazing study sites had disappeared or become (dewatering, nonnative species, p. 247); rates were 5 to 30 times higher in so polluted that they could no longer the Rı´o Papaloapan (pollution, p. 252); riparian areas than on the uplands, support fishes. Only 15 percent of the lagos de Zacapu and Yuriria (habitat which may be due in part to several sites were still capable of supporting destruction, p. 282); and the Rı´o Pa´nuco factors: (1) Higher forage volume and sensitive species. Forty percent (17 Basin (nonnative species, p. 295). palatability of species in riparian areas; different species) of the native fishes of Conant (1974, pp. 486–489) described (2) water availability; (3) the close the basin had suffered major declines in significant threats to northern Mexican proximity of riparian areas to the best distribution, and three species may be gartersnake habitat within its upland grazing sites; and (4) extinct. The extent and magnitude of distribution in western Chihuahua, microclimatic features such as cooler degradation in the Rı´o Lerma basin Mexico, and within the Rio Concho temperatures and shade (Trimble and matches or exceeds the worst cases system where it occurs. These threats Mendel 1995, p. 244). reported for comparably sized basins included impoundments, water Effects of improper livestock elsewhere in the world.’’ diversions, and purposeful management on riparian and aquatic Several rivers within the historical introductions of largemouth bass, communities have spanned from early range of the northern Mexican common carp, and bullfrogs. We discuss settlement to modern day. Some gartersnake have been impounded and the threats from nonnative species historical accounts of riparian area dammed throughout Mexico, resulting introductions below in our discussion of conditions in Arizona clarify early in habitat modification and the Factor C. effects of poor livestock management. dispersal and establishment of Clearly, water quality and quantity are Cheney et al. (1990, pp. 5, 10) provide nonnative species. The damming and being affected by ongoing activities in historical accounts of the early adverse modification of the lower Colorado the United States and Mexico. Due to effects of improper livestock River in Mexico, where the northern the reliance of the northern Mexican management in the riparian zones and Mexican gartersnake occurred, has gartersnake on ecosystems and adjacent uplands of the Tonto National facilitated the replacement of the entire communities supported by permanent Forest and in south-central Arizona. native fishery with nonnative species water sources, these threats are These accounts describe the removal of (Miller et al. 2005, p. 61). Nonnative significant to the survival and viability riparian trees for preparation of species continue to pose significant of existing and future northern Mexican livestock use and substantial changes to threats in the decline of native, often gartersnake populations. flow regimes accentuated by observed highly localized, prey species of the Improper Livestock Grazing and increases in runoff and erosion rates. northern Mexican gartersnake, as Agricultural Uses. In a number of ways Such accounts of riparian conditions discussed further in Factor C below described below, poorly managed within the historical distribution of the (Miller et al. 2005, p. 60). livestock grazing has damaged northern Mexican gartersnake in Miller et al. (2005) provide approximately 80 percent of stream, Arizona contribute to the understanding information on threats to freshwater cienega, and riparian ecosystems in the of when declines in abundance and fishes, and riparian and aquatic western United States (Kauffman and distribution may have occurred and the communities in specific waterbodies Krueger 1984, pp. 433–435; Weltz and contributions of this factor to the throughout Mexico that are within the Wood 1986, pp. 367–368; Waters 1995, subsequent fragmentation of historical range of the northern Mexican pp. 22–24; Pearce et al. 1998, p. 307; populations and widespread gartersnake: The Rı´o Grande (dam Belsky et al. 1999, p. 1). Fleischner extirpations. construction, p. 78 and extirpations of (1994, p. 629) found that ‘‘Because Poor livestock management causes a freshwater fish species, pp. 82, 112); livestock congregate in riparian decline in diversity, abundance, and headwaters of the Rı´o Lerma ecosystems, which are among the most species composition of riparian (extirpation of freshwater fish species, biologically rich habitats in arid and herpetofauna communities from direct nonnative species, pollution, semiarid regions, the ecological costs of or indirect threats to the prey base, the dewatering, pp. 60, 105, 197); Lago de grazing are magnified at these sites.’’ habitat, or to the northern Mexican
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gartersnake. These effects include: (1) from Dugas Road to Little Ash Creek, Alternatively, well-managed stock tanks Declines in the structural richness of the along Little Ash Creek from Brown can provide habitat suitable for northern vegetative community; (2) losses or Spring to Dry Creek, along Sycamore Mexican gartersnakes both structurally reductions of the prey base; (3) Creek in the vicinity of its confluence and in terms of prey base, especially increased aridity of habitat; (4) loss of with the Verde River, and on potential when the tank remains devoid of thermal cover and protection from northern Mexican gartersnake habitat nonnative species while supporting predators; and (5) a rise in water along Pinto Creek at the confluence with native prey species; provides adequate temperatures to levels lethal to larval the West Fork of Pinto Creek. In vegetation cover; and provides reliable stages of amphibian and fish southeastern Arizona, there have been water sources in periods of prolonged development (Szaro et al. 1985, p. 362; observations of effects to the vegetative drought. Given these benefits of well- Schulz and Leininger 1990, p. 295; community suggesting that livestock managed stock tanks, we believe well- Belsky et al. 1999, pp. 8–11). Improper grazing activities continue to adversely managed stock tanks may be an livestock grazing may also lead to affect remaining populations of northern important component to northern desertification (the process of becoming Mexican gartersnakes by reducing or Mexican gartersnake conservation. arid land or desert as a result of land eliminating cover required by the Direct mortality of amphibian species, mismanagement or climate change) due northern Mexican gartersnake for in all life stages, from being trampled by to a loss in soil fertility from erosion thermoregulation, protection from livestock has been documented in the and gaseous emissions spurred by a predation, and foraging (Hale 2001, pp. literature (Bartelt 1998, p. 96; Ross et al. reduction in vegetative ground cover 32–34, 50, 56). 1999, p. 163). The resultant extirpation (Schlesinger et al. 1990, p. 1043). To increase forage and stocking rates risk of amphibian populations as a prey Szaro et al. (1985, p. 360) assessed the for livestock production in the arid base for northern Mexican gartersnakes effects of improper livestock lowlands of northern Mexico, African by direct mortality is governed by the management on a sister taxon. They buffelgrass was widely introduced in relative isolation of the amphibian found that western (terrestrial) Mexico and has subsequently spread via population, the viability of that gartersnake (Thamnophis elegans its own natural means of dispersal population, and the propensity for vagrans) populations were significantly (Bu´ rquez-Montijo et al. 2002, p. 131; stochastic events such as wildfires. higher (versus controls) in terms of Nijhuis 2007, pp. 1–7). Buffelgrass Livestock grazing within habitat abundance and biomass in areas that invasions pose a serious threat to native occupied by northern Mexican were excluded from grazing, where the arid ecosystems because buffelgrass gartersnakes can result in direct streamside vegetation remained lush, prevents germination of native plant mortality of individual gartersnakes as than where uncontrolled access to species, competes for water, crowds out observed in a closely related taxon on grazing was permitted. This effect was native vegetation, and creates fine fuels the Apache-Sitgreaves National Forest. complemented by higher amounts of in vegetation communities not adapted In that instance, a black-necked cover from organic debris from ungrazed to fire. In such native arid ecosystems, gartersnake (Thamnophis cyrtopsis shrubs that accumulate as the debris buffelgrass has caused many changes, cyrtopsis) had apparently been killed by moves downstream during flood events. including severe soil erosion resulting trampling by cattle along the shore of a Specifically, results indicated that snake from an increase in the number and stock tank within an actively grazed abundance and biomass were severity of fires (Bu´ rquez-Montijo et al. allotment (Chapman 2005). This event significantly higher in ungrazed habitat, 2002, pp. 135, 138). Erosion affects the was not observed first-hand, but was with a five-fold difference in number of suitability of habitat for northern supported by postmortem photographic snakes captured, despite the difficulty Mexican gartersnakes and their prey documentation of the physical injuries of making observations in areas of species by increasing the turbidity of to the specimen and the location of the increased habitat complexity (Szaro et streams and filling in important pool carcass among a dense cluster of hoof al. 1985, p. 360). Szaro et al. (1985, p. habitat, which increases the water tracks along the shoreline of the stock 362) also noted the importance of temperature of pools, lowers the tank. It is also unlikely that a predator riparian vegetation for the maintenance dissolved oxygen content of the water, would kill the snake and leave it of an adequate prey base and as cover and reduces their permanency. Recent uneaten. While this type of direct in thermoregulation and predation estimates indicate that 80 percent of mortality of gartersnakes has long been avoidance behaviors, as well as for Mexico is affected by soil erosion suspected by agency biologists and foraging success. caused by vegetation removal related to academia, this may be the first recorded Watersheds where improper grazing grazing, fires, agriculture, deforestation, observation of direct mortality of a has been documented as a contributing etc. The most serious erosion is gartersnake due to livestock trampling. factor of northern Mexican gartersnake occurring in the States of Guanajuato We expect this type of direct mortality declines include the Verde, Salt, Agua (43 percent of the State’s land area), to be uncommon but significant in the Fria, San Pedro, Gila, and Santa Cruz Jalisco (25 percent of the State’s land instance of a fragmented population (Hendrickson and Minckley 1984, pp. area), and Me´xico (25 percent of the with a skewed age-class distribution 140, 152, 160–162; Rosen and Schwalbe State’s land area) (va Landa et al. 1997, (large adults), without a neighboring 1988, pp. 32–33; Girmendock and p. 317), the states in which the northern source population to assist with Young 1997, p. 47; Voeltz 2002, pp. 45– Mexican gartersnake occurs. recolonization, and low to no 81; Krueper et al. 2003, pp. 607, 613– The effects of stock tanks associated recruitment as currently observed in 614; Holycross et al. 2006, pp. 52–61; with livestock grazing on northern many northern Mexican gartersnake McKinnon 2006d, 2006e; Paradzick et Mexican gartersnakes depend on how populations in the United States. In al. 2006, pp. 90–92; USFS 2008). they are managed. Dense bank and these circumstances, the loss of one or Holycross et al. (2006, pp. 53–55, 58) aquatic vegetation is an important more adults, most notably reproductive recently documented adverse effects habitat characteristic for the northern females, may lead directly to extirpation from improper livestock grazing on Mexican gartersnake that can be affected of the species from a given site with no northern Mexican gartersnake habitat if the impoundment is poorly managed, expectation of recolonization. along the Agua Fria from EZ Ranch to which may lead to trampling or Poor forestry and agricultural Bloody Basin Road, along Dry Creek overgrazing of the bankside vegetation. practices were cited as the largest and
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most widespread threats to the native associated with physical disturbances to ecosystems and increased the fisheries of the Jalisco and Colima area its habitat, such as livestock grazing, probability of devastating wildfires. The in Mexico investigated by Lyons and when the biotic community is effects of these catastrophic wildfires Navarro-Perez (1990, p. 37), affecting comprised of wholly native species. include the removal of vegetation, the prey availability for northern Mexican However, even modest alterations in the degradation of watershed condition, gartersnakes in areas where they occur. physical habitat of the northern altered stream behavior, and increased Lyons and Navarro-Perez (1990, p. 37) Mexican gartersnake may lead to sedimentation of streams. These effects indicated that in high-elevation areas, population declines, or even can harm fish communities, as observed clear-cutting of trees and unrestricted extirpations, when these adverse effects in the 1990 Dude Fire, when livestock grazing have increased erosion act in combination with the adverse corresponding ash flows decimated and sedimentation. They suspected effects of nonnative species. In Mexico, some fish populations in Dude Creek impacts on fish and invertebrate livestock grazing, often in association and the East Verde River (Voeltz 2002, populations had occurred. In lowland with deforestation and crop cultivation, p. 77), which, ultimately, affects habitat areas, Lyons and Navarro-Perez (1990, are also having adverse affects on the suitability for the gartersnake. These p. 37) cited diversion of water for northern Mexican gartersnake. We effects can significantly reduce the prey irrigation, runoff from cultivated fields, recognize that well-managed grazing can base for northern Mexican gartersnakes and runoff from small towns and occur with limited effects to this species and could lead to direct mortality in the villages as causing additional when the presence or absence of case of high-intensity fires that are environmental degradation. Lyons and nonnative species is considered, and within occupied habitat. The Chiricahua Navarro-Perez (1990, p. 37) found that management emphasis is directed leopard frog recovery plan cites altered the tolerance of several fish species to towards limiting some access to riparian fire regimes as a serious threat to degradation depended on the form of and aquatic habitats within occupied Chiricahua leopard frogs, a prey species degradation. habitat. These actions, combined with for northern Mexican gartersnakes Minckley et al. (2002, pp. 687–705) management that disperses livestock (USFWS 2008, pp. 38–39). described three new species of pupfish away from riparian areas, reduce the Fire has also become an increasingly and provided a summary of threats (p. threats of livestock grazing on northern significant threat in lower elevation 696) to these species and their habitat in Mexican gartersnakes and their habitats. communities as well. Esque and Chihuahua, Mexico, within the As previously stated, we also recognize Schwalbe (2002, pp. 180–190) discuss distribution of the northern Mexican well-managed stock tanks as a valuable the effect of wildfires in the upper and gartersnake. Initial settlement and tool in the conservation of northern lower subdivisions of Sonoran agricultural development of the area Mexican gartersnakes. desertscrub where the northern Mexican resulted in significant channel cutting Additional information on the effects gartersnake historically occurred. The through soil layers protecting the of improper livestock grazing to the widespread invasion of nonnative alluvial plain above them, which northern Mexican gartersnake and its annual grasses, such as brome species resulted in reductions in the base level habitat can be found in our 2006, 12- (Bromus sp.) and Mediterranean grasses of each basin in succession (Minckley et month finding for this species (71 FR (Schismus sp.), appear to be largely al. 2002, p. 696). Related to these 56227) and in Sartz and Tolsted (1974, responsible for altered fire regimes that activities, the building of dams and p. 354); Szaro et al. (1985, pp. 360, 362, have been observed in these diversion structures dried entire reaches 364); Weltz and Wood (1986, pp. 367– communities, which are not adapted to of some regional streams and altered 368); Rosen and Schwalbe (1988, pp. fire (Esque and Schwalbe 2002, p. 165). flow patterns of others (Minckley et al. 32–33, 47); Clary and Webster (1989, p. African buffelgrass (Pennisetum ciliare) 2002, p. 696). This was followed by 1); Clary and Medin (1990, p. 1); Schulz is recognized as another invading groundwater pumping (enhanced by the and Leininger (1990, p. 295); nonnative plant species throughout the invention of the electric pump) which Schlesinger et al. (1990, p. 1043); lower elevations of northern Mexico and lowered groundwater levels and dried- Orodho et al. (1990, p. 9); Fleischner Arizona. Nijhuis (2007, pp. 1–7) discuss up springs and small channels and (1994, pp. 629, 631–632); Trimble and the spread of nonnative buffelgrass reduced the reliability of baseflow in Mendel (1995, pp. 235–236, 243–244); within the Sonoran Desert of Arizona ‘‘essentially all systems’’ (Minckley et Pearce et al. (1998, p. 302); Belsky et al. and adjoining Mexico, citing the grass’ al. 2002, p. 696). Subsequently, the (1999, pp. 8–11); Stromberg and Chew ability to out compete native vegetation introduction and expansion of (2002, p. 198); and Krueper et al. (2003, and present significant risks of fire in an nonnative species in the area pp. 607, 613–614). ecosystem that is not adapted to fire. In successfully displaced or extirpated High-Intensity Wildfires. Low- areas comprised entirely of native many native species (Minckley et al. intensity fire has been a natural species, ground vegetation density is 2002, p. 696). disturbance factor in forested mediated by barren spaces that do not Our analysis of the best available landscapes for centuries, and low- allow fire to carry itself across the scientific and commercial information intensity fires were common in landscape. However, in areas where available indicates that adverse effects southwestern forests prior to European nonnative grasses have become from improper livestock management on settlement (Rinne and Neary 1996, pp. established, the fine fuel load is the northern Mexican gartersnake, its 135–136). Rinne and Neary (1996, p. continuous, and fire is capable of habitat, and its prey base can be 143) discuss the current effects of fire spreading quickly and efficiently (Esque significant, especially when combined management policies on aquatic and Schwalbe 2002, p. 175). with other threats, most notably communities in Madrean Oak After disturbances such as fire, nonnative species (discussed below Woodland biotic communities in the nonnative grasses may exhibit dramatic under Factor C). Preliminary gartersnake southwestern United States. They population explosions, which hasten survey data from Burger (2008) from the concluded that existing wildfire their effect on native vegetative States of Durango and southern suppression policies intended to protect communities. Additionally, with Chihuahua, Mexico, indicate that the the expanding number of human increased fire frequency, these northern Mexican gartersnake is less structures on forested public lands have population explosions ultimately lead to susceptible to population impacts altered the fuel loads in these a type-conversion of the vegetative
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community from desertscrub to of streamside soils, and the destruction 2006, p. 95). Due to the immediate grassland (Esque and Schwalbe 2002, and removal of riparian vegetation proximity of the upper Santa Cruz River pp. 175–176). Fires carried by the fine necessary as cover for the northern to the international border and the effect fuel loads created by nonnative grasses Mexican gartersnake. Current border of border control operations that funnel often burn at unnaturally high infrastructure projects, including undocumented immigrants into rural temperatures, which may result in soils vehicle barriers and pedestrian fences, environments, we conclude that these becoming hydrophobic (water are located specifically in valley adverse effects likely occur in this area, repelling), exacerbate sheet erosion, and bottoms and have resulted in direct which is occupied by the northern contribute large amounts of sediment to impacts to water courses and altered Mexican gartersnake. receiving water bodies, thereby affecting drainage patterns affecting northern Threats from illegal border crossers the health of the riparian community Mexican gartersnake habitat (USFWS appear to have increased in recent years (Esque and Schwalbe 2002, pp. 177– 2008, p. 4). These activities also within the Coronado National Forest of 178). The siltation of isolated, remnant produce sediment in streams, which southern Arizona (USFS 2008). Reports pools in intermittent streams affects their suitability as habitat for of significant water pollution from significantly affects lower elevation prey species of the northern Mexican bathing activities by undocumented species by increasing the water gartersnake by reducing their immigrants in habitat occupied by temperature, reducing dissolved oxygen, permanency and altering their physical northern Mexican gartersnakes have and reducing or eliminating the and chemical parameters. Riparian areas been received (USFS 2008). Of permanency of pools, as observed in along the upper San Pedro River have particular concern to USFS (2008), was pools occupied by lowland leopard been impacted by abandoned fires that the concentrated use of pools by frogs and native fish, important prey undocumented immigrants started to undocumented immigrants during the species for northern Mexican keep warm or prepare food (Segee and warmest months before summer rains gartersnakes (Esque and Schwalbe 2002, Neeley 2006, p. 23). There is also the commence, when the habitat is also p. 190). threat of pursuit, capture, and death of critical to the northern Mexican Undocumented Immigration and northern Mexican gartersnakes when gartersnake and its prey. The amount of International Border Enforcement and they are encountered by illegal border surface water is generally considered Management. Undocumented crossers and border enforcement the lowest during the early summer, immigrants and smugglers attempt to personnel in high-use areas due to the pre-monsoon months in Arizona, which cross the International border from snake’s stigma in society (Rosen and compounds the effects of the use of Mexico into the United States in areas Schwalbe 1988, p. 43; Ernst and Zug pools for bathing by concentrating water historically and currently occupied by 1996, p. 75; Green 1997, pp. 285–286; contamination in the limited habitat the northern Mexican gartersnake. Nowak and Santana-Bendix 2002, p. available to northern Mexican These illegal border crossings and the 39). gartersnakes and their prey species. corresponding efforts to enforce U.S. Because of the limited amount of border laws and policies have been The wetland habitat within the San alternative habitat, illegal border occurring for many decades with Bernardino National Wildlife Refuge crossers and gartersnakes are increasing intensity and have resulted provides habitat for the northern concentrated in the same areas, in unintended adverse effects to biotic Mexican gartersnake, where it is now increasing encounter rates and the communities in the border region. likely extirpated, and has been potential threats to northern Mexican During the warmest months of the year, adversely affected by undocumented gartersnakes. many attempted border crossings occur immigration. It is estimated that Summary of Factor A. Riparian and in riparian areas that serve to provide approximately 1,000 undocumented aquatic habitats that are essential for the shade, water, and cover. Increased U.S. immigrants per month use these survival of the northern Mexican border enforcement efforts that began in important wetlands for bathing, gartersnake are being negatively the early 1990s in California and Texas drinking, and other uses during their impacted throughout the subspecies’ have resulted in a shift in crossing journey northward (Segee and Neeley range. Threats including water patterns and increasingly concentrated 2006, pp. 21–22). These activities occur diversions, groundwater pumping, levels of attempted illegal border in other border areas, such as the Santa dams, channelization, and erosion- crossings into Arizona (Segee and Cruz River, where the northern Mexican related effects are occurring in both the Neeley 2006, p. 6). gartersnake occurs, although they have United States and Mexico that affect the Riparian habitats that historically not been quantified (Segee and Neeley amount of water within occupied supported or may currently support 2006, pp. 21–22). They can contaminate northern Mexican gartersnake habitat, northern Mexican gartersnakes in the the water quality of the wetlands and directly affecting its suitability for San Bernardino National Wildlife lead to reductions in the prey base for northern Mexican gartersnakes. Threats Refuge, the San Pedro River corridor, the northern Mexican gartersnake, as from development, roads, flood control the Santa Cruz River corridor, the lower well as increase exposure of the snake and water diversion, improper livestock Colorado River corridor, and along to humans, and thereby increase direct grazing, high-intensity wildfire, and many smaller streamside and canyon mortality rates (Rosen and Schwalbe undocumented immigration that alter bottom areas within Cochise, Santa 1988, p. 43; Ernst and Zug 1996, p. 75; the vegetation of occupied northern Cruz, and Pima counties have high Green 1997, pp. 285–286; Nowak and Mexican gartersnake habitat are levels of undocumented immigrant Santana-Bendix 2002, p. 39; Segee and documented throughout its range and traffic (Segee and Neeley 2006, Neeley 2006, pp. 21–22). In addition, reduce the habitat’s suitability as cover Executive Summary, pp. 10–12, 21–23). numerous observations of littering and for protection from predators, as a Traffic on new roads and trails from destruction of vegetation and wildlife foraging area, and as an effective illegal border crossing and enforcement occur annually throughout the San thermoregulatory site. However, activities, as well as the construction, Bernardino National Wildlife Refuge, Rorabaugh (2008, p. 26) suggests that an use, and maintenance of enforcement which adversely affect the quality and increased awareness of the potential for infrastructure (i.e., fences, walls, and quantity of vegetation as habitat for the ecotourism to provide rural economic lighting systems), leads to compaction northern Mexican gartersnake (USFWS growth is occurring in many areas
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within Sonora, Mexico, which may Disease and nonnative parasites have bumps was not identified or speculated provide enhanced opportunities for been implicated in the decline in the upon, nor were there any signs of conservation of biologically rich prey base of the northern Mexican trauma to their body in these areas. Dr. ecosystems in the future. gartersnake. Particularly, the outbreak of Jim Jarchow, a veterinarian with Nonnative plant species, in particular chytridiomycosis or ‘‘Bd,’’ a skin fungus herpetological expertise, reviewed shrubs (genus Tamarix) and buffelgrass, (Batrachochytrium dendrobatidis), has photographs of affected specimens and are increasing their distribution in both been identified as a chief causative suggested the bumps may likely contain the United States and Mexico and agent in the significant declines of many plerocercoid larvae of a adversely affect habitat suitability and of the native ranid frogs and other pseudophyllidean tapeworm (possibly availability for the northern Mexican amphibian species, and regional Spirometra spp.), which are common in gartersnake. concerns exist for the native fish fish- and frog-eating gartersnakes. This community due to nonnative parasites may not be detrimental to their health B. Overutilization for Commercial, such as the Asian tapeworm provided the bumps do not grow large Recreational, Scientific, or Educational (Bothriocephalus achelognathi) in enough to impair movement or other Purposes southeastern Arizona (Rosen and bodily functions (Boyarski 2008b, p. 8). The northern Mexican gartersnake Schwalbe 1997, pp. 14–15; 2002c, pp. However, Gu´ zman (2008, p. 102) may not be collected in the United 1–19; Morell 1999, pp. 728–732; Sredl documented the first observation of States without special authorization by and Caldwell 2000, p. 1; Hale 2001, pp. mortality of a Mexican gartersnake from the Arizona Game and Fish Department 32–37; Bradley et al. 2002, p. 206). Bd a larval Eustrongylides sp. or the New Mexico Department of Game has been implicated in both large-scale (endoparasitic nematode) which ‘‘raises and Fish. We have found no evidence declines and local extirpations of many the possibility that infection of Mexican that current or historical levels of lawful amphibians, chiefly anuran species, gartersnakes by Eustrongylides sp. or unlawful field collecting of northern around the world (Johnson 2006, p. larvae might cause mortality in some Mexican gartersnakes has played a 3011). Lips et al. (2006, pp. 3166–3169) wild populations,’’ especially in the significant role in the decline of this suggest that the high virulence and large presence of other threats. species. The Arizona Game and Fish number of potential hosts make Bd a Nonnative Species Interactions. A serious threat to amphibian diversity. In Department recently produced host of native predators prey upon Arizona, Bd infections have been identification cards for distribution that northern Mexican gartersnakes reported in several northern Mexican provide information to assist with the including birds of prey, other snakes gartersnake native prey species within field identification of each of Arizona’s [kingsnakes (Lampropeltis sp.), the distribution of the snake (Morell five native gartersnake species, as well whipsnakes (Masticophis sp.), etc.], 1999, pp. 731–732; Sredl and Caldwell as guidance on submitting photographic wading birds, raccoons (Procyon lotor), 2000, p. 1; Hale 2001, pp. 32–37; vouchers for university museum skunks (Mephitis sp.), and coyotes Bradley et al. 2002, p. 207; USFWS collections. Additionally, Arizona State (Canis latrans) (Rosen and Schwalbe 2002a, pp. 40802–40804; USFWS 2007, University and the University of 1988, p. 18). Historically, large, highly pp. 26, 29–32). Declines of native prey Arizona recently began to accept species of the northern Mexican predatory native fish species such as photographic vouchers, versus physical gartersnake from Bd infections have Colorado pikeminnow may have preyed specimens, in their respective museum contributed to the decline of this species upon northern Mexican gartersnakes collections, which will reduce the in the United States and likely in where the two species co-occurred. amount of collection. We believe these Mexico (Morell 1999, pp. 731–732; However, nonnative species represent measures reduce the necessity for field Sredl and Caldwell 2000, p. 1; Hale the most serious threat to the northern biologists to collect physical specimens 2001, pp. 32–37; Bradley et al. 2002, p. Mexican gartersnake through direct (unless discovered postmortem) for 207; USFWS 2002a, pp. 40802–40804; predation and predation on northern locality voucher purposes and, USFWS 2007, pp. 26, 29–32). Mexican gartersnake prey (competition). therefore, further reduce impacts to Research shows that, in a pure Nonnative species, such as the bullfrog, vulnerable populations of the northern culture, the fungus Batrachochytrium the northern (virile) crayfish Mexican gartersnake. We were unable to can grow on boiled snakeskin (keratin), (Orconectes virilis) and red swamp obtain information about the effect of which indicates the potential for the (Procambarus clarki) crayfish, and overutilization for commercial, fungus to live on gartersnake skin in the numerous species of nonnative sport recreational, scientific, or educational wild, if other components of the and bait fish species continue to be the purposes in Mexico. Specific discussion ecosystem are favorable (Longcore et al. most significant threat to the northern of the regulatory protections for the 1999, p. 227). Despite the demonstrated Mexican gartersnake and to its prey base northern Mexican gartersnake is potential, no reports of the organism on from direct predation, competition, and provided under Factor D ‘‘Inadequacy of reptilian hosts in the wild have been modification of habitat (Meffe 1985, pp. Existing Regulatory Mechanisms’’ documented. We, as well as other 179–185; Rosen and Schwalbe 1988, pp. below. researchers, will monitor the incidence 28, 32; 1997, p. 1; Bestgen and Propst 1989, pp. 409–410; Clarkson and C. Disease or Predation of this disease in gartersnakes in the wild for early detection purposes and to Rorabaugh 1989, pp. 531, 535; Marsh Disease. Disease in northern Mexican determine the status of this potential and Minckley 1990, p. 265; Stefferud gartersnakes has not yet been threat. and Stefferud 1994, p. 364; Douglas et documented as a specific threat in the Parasites have been observed in al. 1994, pp. 9–19; Rosen et al. 1995, pp. United States or Mexico. However, northern Mexican gartersnakes. 257–258; 1996b, pp. 2, 11–13; 2001, p. because little is known about disease in Boyarski (2008b, pp. 5–6) recorded 2; Degenhardt et al. 1996, p. 319; wild snakes, it is premature to conclude several snakes within the population at Fernandez and Rosen 1996, pp. 8, 23– that there is no disease threat that could the Page Springs and Bubbling Ponds 27; Richter et al. 1997, pp. 1089, 1092; directly affect remaining northern fish hatcheries with interior bumps or Weedman and Young 1997, p. 1, Mexican gartersnake populations (Rosen bulges along the anterior one-third of Appendices B, C; Inman et al. 1998, p. 2006). the body although the cause of these 17; Rinne et al. 1998, pp. 4–6; Minckley
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et al. 2002, p. 696; DFT 2003, p. 1; species of fish, amphibians, and crayfish al. 2005, pp. 34, 34–41; Olden and Poff Clarkson et al. 2005, p. 20; Fagan et al. are intentionally or unintentionally 2005, pp. 82–87; Holycross et al. 2006, 2005, pp. 34, 34–41; Olden and Poff stocked by anglers and private pp. 13–15, 52–61; Brennan and 2005, pp. 82–87; Turner 2006, p. 10; landowners (Rosen et al. 2001, p. 24). Holycross 2006, p. 123; USFWS 2007, Holycross et al. 2006, pp. 13–15; The management of stock tanks is an pp. 22–23; Caldwell 2008a, 2008b; Jones Brennan and Holycross 2006, p. 123; important consideration for northern 2008b; d’Orgeix 2008; Haney et al. 2008, USFWS 2007, pp. 22–23; Caldwell Mexican gartersnakes. Stock tanks p. 59; Luja and Rodrı´guez-Estrella 2008, 2008a, 2008b; Jones 2008b; d’Orgeix associated with livestock grazing can be pp. 17–22; Rorabaugh 2008, p. 25; USFS 2008; Haney et al. 2008, p. 59; Luja and intermediary ‘‘stepping stones’’ in the 2008; Wallace et al. 2008, pp. 243–244; Rodrı´guez-Estrella 2008, pp.. 17–22; dispersal of nonnative species from Witte et al. 2008, p. 1). Rorabaugh 2008, p. 25; USFS 2008; larger source populations to new areas Declines in the Northern Mexican Wallace et al. 2008, pp. 243–244; Witte (Rosen et al. 2001, p. 24). Gartersnake Anuran Prey Base. Declines et al. 2008, p. 1). The northern Mexican gartersnake in the native leopard frog populations in Riparian and aquatic communities in appears to be particularly vulnerable to Arizona have contributed to declines in both the United States and Mexico have a loss in native prey species (Rosen and the northern Mexican gartersnake as a been dramatically impacted by a shift in Schwalbe 1988, p. 20). Rosen et al. primary native predator. Native ranid species’ composition, from being (2001, pp. 10, 13, 19) examined this frog species such as lowland leopard historically dominated by native fauna issue in detail and proposed two frogs, northern leopard frogs, and to being increasingly occupied by an reasons for the decline in northern federally threatened Chiricahua leopard expanding assemblage of nonnative Mexican gartersnakes following the loss frogs have all experienced significant animal species that have been or decline in the native prey base: (1) declines throughout their distribution in intentionally or accidentally introduced, The species is unlikely to increase the Southwest, partially due to such as crayfish, bullfrogs, sportfish, foraging efforts at the risk of increased predation and competition with and domestic pets. For example, in two predation; and (2) the species needs nonnative species (Clarkson and of eight cases of northern Mexican substantial food regularly to maintain its Rorabaugh 1989, pp. 531, 535; Hayes gartersnake mortality collected at weight and health. If forced to forage and Jennings 1986, p. 490). Rosen et al. Bubbling Ponds Hatchery since 2006, more often for smaller prey items, a (1995, pp. 257–258) found that the cause of death was considered to be reduction in growth and reproductive Chiricahua leopard frog distribution in from domestic cats (Boyarski 2008a). rates can result (Rosen et al. 2001, pp. the Chiricahua Mountain region of The population of northern Mexican 10, 13). Rosen et al. (2001, p. 22) Arizona was inversely related to gartersnakes at the hatcheries occurs concluded that the presence and nonnative species distribution and with potential and known nonnative expansion of nonnative predators without corrective action, predicted that predators including rainbow and brown (mainly bullfrogs, crayfish, and green the Chiricahua leopard frog will be trout, largemouth and smallmouth bass, sunfish) are the primary causes of extirpated from this region. Along the bluegill, crayfish (in Oak Creek), and decline in northern Mexican Mogollon Rim, Holycross et al. (2006, p. bullfrogs (Boyarski 2008b, pp. 3–4, 8). gartersnakes and their prey in 13) found that only 8 sites of 57 Seven snakes (11 percent of those southeastern Arizona. surveyed (15 percent) consisted of an captured) were observed as having some The decline of the northern Mexican entirely native anuran community and level of tail damage, presumably from gartersnake within its historical and that native frog populations in another bullfrog predation attempts and were currently occurring distribution was 19 sites (33 percent) had been noted as having a lower body condition subsequent to the declines in its prey completely displaced by invading index (an indicator of overall health base (native amphibian and fish bullfrogs. based on a set of pre-determined populations) from predation following Scotia Canyon in the Huachuca variables) (Boyarski 2008b, pp. 5, 8). introductions of nonnative bullfrogs, Mountains of southeastern Arizona is a The relatively low occurrence of tail crayfish, and numerous species of exotic location where corresponding declines damage, as compared to the 78 percent sport and bait fish as documented in an of leopard frog and northern Mexican of snakes with tail damage found by extensive body of literature (Nickerson gartersnake populations have been Rosen and Schwalbe (1988, pp. 28–31), and Mays 1970, p. 495; Hulse 1973, p. documented through repeated survey may indicate (1) adequate vegetation 278; Vitt and Ohmart 1978, p. 44; Meffe efforts over time (Holm and Lowe 1995, density was used by gartersnakes to 1985, pp. 179–185; Ohmart et al. 1988, p. 33). Surveys of Scotia Canyon avoid bullfrog predation attempts; (2) a pp. 143–147; Rosen and Schwalbe 1988, occurred during the early 1980s and relatively low density population of pp. 28–31; 1997, pp. 8–16; Bestgen and again during the early 1990s. Leopard bullfrogs occurs at the site (bullfrog Propst 1989, pp. 409–410; Clarkson and frogs in Scotia Canyon were population density data were not Rorabaugh 1989, pp. 531–538; Marsh infrequently observed during the early collected); (3) gartersnakes may not and Minckley 1990, p. 265; Sublette et 1980s and were apparently extirpated need to move significant distances to al. 1990, pp. 112, 243, 246, 304, 313, by the early 1990s (Holm and Lowe achieve foraging success, which might 318; Stefferud and Stefferud 1994, p. 1995, pp. 45–46). Northern Mexican have reduced the potential for 364; Holm and Lowe 1995, p. 5; Rosen gartersnakes were observed in decline encounters with bullfrogs; or, (4) that et al. 1995, pp. 251, 257–258; 1996a, pp. during the early 1980s with low capture gartersnakes infrequently escape 2–3; 1996b, p. 2; 2001, p. 2; Sredl et al. rates remaining through the early 1990s bullfrog predation attempts, were 1995a, pp. 7–8; 1995b, pp. 8–9; 1995c, (Holm and Lowe 1995, pp. 27–35). removed from the population, and were pp. 7–8; 2000, p. 10; Degenhardt et al. Surveys documented further decline in consequently not detected by surveys. 1996, p. 319; Fernandez and Rosen 2000 (Rosen et al. 2001, pp. 15–16). A Additional information on tail damage 1996, pp. 8–27; Drost and Nowak 1997, former large, local population of as an indicator of predation is found in p. 11; Weedman and Young 1997, p. 1, northern Mexican gartersnakes at the our discussion of Factor C below. Appendices B, C; Inman et al. 1998, p. San Bernardino National Wildlife Stock tanks associated with livestock 17; Rinne et al. 1998, pp. 4–6; Turner et Refuge has also experienced a grazing may facilitate the spread of al. 1999, p. 11; Nowak and Spille 2001, correlative decline of leopard frog and nonnative species when nonnative p. 11; Bonar et al. 2004, p. 3; Fagan et northern Mexican gartersnake
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populations, at least in part related to Peloncillo mountains, and the Sulphur of northern Mexican gartersnakes in that illegal immigration and smuggling Springs, San Bernardino, and San area. activities in riparian and aquatic Simon valleys. They found that 43 The widespread decline of native fish habitats as discussed in Factor A above percent of all cold-blooded aquatic and species from the arid southwestern (Rosen and Schwalbe 1988, p. 28; 1995, semi-aquatic vertebrate species detected United States and Mexico has resulted p. 452; 1996, pp. 1–3; 1997, p. 1; 2002b, were nonnative. The most commonly largely from interactions with nonnative pp. 223–227; 2002c, pp. 31, 70; Rosen encountered nonnative species was the species and has been captured in the et al. 1996b, pp. 8–9; 2001, pp. 6–10). bullfrog (Rosen et al. 1995, p. 254). listing rules of 13 native species listed Survey data indicate that declines of Native ranid frogs (particularly under the Act whose historical ranges leopard frog populations, often lowland and Chiricahua leopard frogs), overlap with the historical distribution correlated with nonnative species which are a primary prey species for of the northern Mexican gartersnake. introductions, the spread of northern Mexican gartersnakes, are one Native fish species that were likely prey chytridiomycosis disease, and habitat of the most imperiled taxa of Sonora, species for the northern Mexican modification and destruction, have Mexico, due primarily to threats from gartersnake, including bonytail chub occurred throughout much of the U.S. nonnative species (bullfrogs, crayfish, (Gila elegans, 45 FR 27710, April 23, distribution of the northern Mexican and sport fish) (Rorabaugh 2008, p. 25). 1980), Yaqui catfish (Ictalurus pricei, 49 gartersnake (Nickerson and Mays 1970, Witte et al. (2008, p. 1) found that the FR 34490, August 31, 1984), Yaqui chub p. 495; Vitt and Ohmart 1978, p. 44; disappearance of ranid frog populations (Gila purpurea, 49 FR 34490, August 31, Ohmart et al. 1988, p. 150; Rosen and in Arizona were 2.6 times more likely in 1984), Yaqui topminnow (Poeciliopsis Schwalbe 1988, Appendix I; 1995, p. the presence of crayfish. Witte et al. occidentalis sonoriensis, 32 FR 4001, 452; 1996, pp. 1–3; 1997, p. 1; 2002b, (2008, p. 7) emphasized the significant March 11, 1967), beautiful shiner pp. 232–238; 2002c, pp. 1, 31; Clarkson influence of nonnative species on the (Cyprinella formosa, 49 FR 34490, and Rorabaugh 1989, pp. 531–538; Sredl disappearance of ranid frogs in Arizona. August 31, 1984), humpback chub (Gila et al. 1995a, pp. 7–8; 1995b, pp. 8–9; Declines in the Northern Mexican cypha, 32 FR 4001, March 11, 1967), Gartersnake Native Fish Prey Base. 1995c, pp. 7–8; 2000, p. 10; Holm and Gila chub (Gila intermedia, 70 FR Native fish species such as the federally Lowe 1995, pp. 45–46; Rosen et al. 66663, November 2, 2005), Colorado endangered Gila chub, roundtail chub (a 1996b, p. 2; 2001, pp. 2, 22; Degenhardt pikeminnow (Ptychocheilus lucius, 32 species petitioned for Federal listing), et al. 1996, p. 319; Fernandez and Rosen FR 4001, March 11, 1967), spikedace and federally endangered Gila 1996, pp. 6–20; Drost and Nowak 1997, (Meda fulgida, 51 FR 23769, July 1, topminnow historically were among the p. 11; Turner et al. 1999, p. 11; Nowak 1986) loach minnow (Tiaroga cobitis, 51 primary prey species for the northern and Spille 2001, p. 32; Holycross et al. FR 39468, October 28, 1986), razorback Mexican gartersnake (Rosen and 2006, pp. 13–14, 52–61). Specifically, sucker (Xyrauchen texanus, 56 FR Schwalbe 1988, p. 18). Northern Holycross et al. (2006, pp. 53–57, 59) 54957, October 23, 1991), desert pupfish Mexican gartersnakes depend on native recently documented extirpations of the (Cyprinodon macularius, 51 FR 10842, fish as a principle part of their prey March 31, 1986), and Gila topminnow northern Mexican gartersnake’s native base, although nonnative mosquitofish leopard frog prey base at several (Poeciliopsis occidentalis occidentalis, may also be taken as prey (Holycross et 32 FR 4001, March 11, 1967). In total currently, historically, or potentially al. 2006, p. 23). Both nonnative sport occupied locations including the Agua within Arizona, 19 of 31 (61 percent) of and bait fish compete with the northern native fish species are listed under the Fria River in the vicinity of Table Mesa Mexican gartersnake in terms of its Act. Arizona ranks the highest of all 50 Road and Little Grand Canyon Ranch native fish and native anuran prey base. States in the percentage of native fish and at Rock Springs, Dry Creek from Collier et al. (1996, p. 16) note that species with declining trends (85.7 Dugas Road to Little Ash Creek, Little interactions between native and percent, Stein 2002, p. 21; Warren and Ash Creek from Brown Spring to Dry nonnative fish have significantly Burr 1994, pp. 6–18). Creek, Sycamore Creek (Agua Fria contributed to the decline of many There are significant ongoing threats watershed) in the vicinity of the Forest native fish species from direct predation from nonnative species to the snake in Service Cabin, at the Page Springs and and indirectly from competition (which Mexico. Lyons and Navarro-Perez (1990, Bubbling Ponds fish hatchery along Oak has adversely affected the prey base for pp. 32–46) investigated the fish Creek, Sycamore Creek (Verde River northern Mexican gartersnakes). communities of 17 streams in and watershed) in the vicinity of the Holycross et al. (2006, pp. 53–55) adjacent to the Sierra de Manantla´n confluence with the Verde River north recently documented significantly Biosphere Reserve in Jalisco and of Clarkdale, along several reaches of depressed or extirpated native fish prey Colima, Mexico. They noted the the Verde River mainstem, Cherry Creek bases for the northern Mexican exceptionally high number of native fish on the east side of the Sierra Ancha gartersnake along the Agua Fria in the species with small, localized Mountains, and Tonto Creek from Gisela vicinity of Table Mesa Road and the distributions, which makes them more to ‘‘the Box,’’ near its confluence with Little Grand Canyon Ranch, along Dry susceptible to threats and subsequent Rye Creek. Creek from Dugas Road to Little Ash extirpation, stating that degradation of Rosen et al. (2001, p. 22) identified Creek, along Little Ash Creek from just a few streams could result in the the expansion of bullfrogs into the Brown Spring to Dry Creek, along elimination of many species of fish and, Sonoita grasslands, which border Sycamore Creek (Agua Fria watershed) thus, prey availability for the northern occupied northern Mexican gartersnake in the vicinity of the Forest Service Mexican gartersnake. habitat, and the introduction of crayfish Cabin, and along Sycamore Creek In an evolutionary context, native into Lewis Springs as being of particular (Verde River watershed) in the vicinity fishes co-evolved with very few concern in terms of future recovery of its confluence with the Verde River predatory fish species, whereas many of efforts for the northern Mexican north of Clarkdale. Rosen et al. (2001, the nonnative species co-evolved with gartersnake. Rosen et al. (1995, pp. 252– Appendix I) documented the decline of many predatory species (Clarkson et al. 253) sampled 103 sites in the several native fish species in several 2005, p. 21). A contributing factor to the Chiricahua Mountains region, which locations visited in southeastern decline of native fish species cited by included the Chiricahua, Dragoon, and Arizona, further affecting the prey base Clarkson et al. (2005, p. 21) is that most
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of the nonnative species evolved data indicating that the nonnative red the spiny-rayed fish, are not considered behaviors, such as nest guarding, to shiner may be competitively displacing prey species for the northern Mexican protect their offspring from these many spikedace (a potential prey item of the gartersnake. These nonnative species predators, while native species are northern Mexican gartersnake) in can be difficult to swallow due to their generally broadcast spawners that Arizona and New Mexico within the body shape and spiny dorsal fins. They provide no parental care. In the historical or current distribution of the are predatory on juvenile gartersnakes presence of nonnative species, the northern Mexican gartersnake. and reduce the abundance of or reproductive behaviors of native fish fail In a comprehensive and thorough completely eliminate native fish to allow them to compete effectively assessment of the Verde River, Bonar et populations. This is particularly with the nonnative species and, as a al. (2004, p. 57) found that in the Verde important in the wake of random, high- result, the viability of native fish River mainstem, nonnative fishes were intensity events, such as flooding, populations is reduced. approximately 2.6 times more dense per extreme water temperatures, or Olden and Poff (2005, p. 75) stated unit volume of river than native fishes, excessive turbidity. Native fish are that environmental degradation and the and their populations were adapted to the dramatic fluctuations in proliferation of nonnative fish species approximately 2.8 times that of native water conditions and flow regimes, and threaten the highly localized and unique fishes per unit volume of river. generally persist in the wake of fish faunas of the American Southwest. Haney et al. (2008, p. 61) declared the stochastic events and continue to The fastest expanding nonnative species northern Mexican gartersnake as nearly provide a prey base for the northern are red shiner (Cyprinella lutrensis), lost from the Verde River and suggested Mexican gartersnake. Nonnative fish, fathead minnow (Pimephales promelas), that diminished river flow may be an even species that may be used as prey green sunfish (Lepomis cyanellus), important factor. Differing river flows by the northern Mexican gartersnake, largemouth bass (Micropterus may provide both advantages and generally are ill-adapted to these salmoides), western mosquitofish, and disadvantages to aquatic species. The conditions and may be removed from channel catfish (Ictalurus punctatus). timing, duration, intensity, and the area temporarily or permanently, These species are considered to be the frequency of flood events has been depending on the hydrologic most invasive in terms of their negative altered to varying degrees by the connectivity to current populations. If impacts on native fish communities presence of dams along the Verde River, an area is solely comprised of nonnative (Olden and Poff 2005, p. 75). Many which has an effect on fish fish, the northern Mexican gartersnake nonnative fishes in addition to those communities. Specifically, Haney et al. may be faced with nutritional stress or listed immediately above, including (2008, p. 61) suggested that flood pulses starvation because only a few small- yellow and black bullheads (Ameiurus may help to reduce populations of bodied, soft-rayed fish species are taken sp.), flathead catfish (Pylodictis nonnative species (see discussion as prey and significant effort may be below) and efforts to increase the olivaris), and smallmouth bass required to obtain these species. (Micropterus dolomieue), have been baseflows may assist in sustaining introduced into formerly and currently native prey species for the northern Clarkson et al. (2005) discuss occupied northern Mexican gartersnake Mexican gartersnake. However, the management conflicts as a primary habitat and are predators on northern investigators also suggest that, because factor in the decline of native fish Mexican gartersnakes and their prey the northern Mexican gartersnake preys species in the southwestern United (Bestgen and Propst 1989, pp. 409–410; on both fish and frogs, it may be less States and declare the entire native Marsh and Minckley 1990, p. 265; affected by reductions in baseflow but fauna as imperiled. The investigators Sublette et al. 1990, pp. 112, 243, 246, might incur greater risks from cite nonnative species as the most 304, 313, 318; Abarca and Weedman concentrating nonnative predators and consequential factor that has led to 1993, pp. 6–12; Stefferud and Stefferud higher water-borne disease rates (Haney rangewide declines that prevents or 1994, p. 364; Weedman and Young et al. 2008, pp. 82, 93). negates species’ recovery efforts from 1997, pp. 1, Appendices B, C; Rinne et The Desert Fishes Team (DFT) is an being implemented or being successful al. 1998, pp. 3–6; Voeltz 2002, p. 88; ‘‘independent group of biologists and (Clarkson et al. 2005, p. 20). Clarkson et Bonar et al. 2004, pp. 1–108; Fagan et parties interested in protecting and al. (2005, p. 20) note that over 50 al. 2005, pp. 34, 38–39, 41). conserving native fishes of the Colorado nonnative species have been introduced Several authors have identified both River basin’’ and includes personnel into the Southwest as either sportfish or the presence of nonnative fish as well as from the U.S. Forest Service, U.S. baitfish and are still being actively their deleterious effects on native Bureau of Reclamation, U.S. Bureau of stocked, managed for, and promoted by species within Arizona. Abarca and Land Management, University of both Federal and State agencies as Weedman (1993, pp. 6–12) found that Arizona, Arizona State University, the nonnative recreational fisheries. To help the number of nonnative fish species Nature Conservancy, and independent resolve the conflicting management was twice the number of native fish experts (DFT 2003, p. 1). DFT (2003, p. mandates of native fish recovery and the species in Tonto Creek in the early 1) declared the native fish fauna of the promotion of recreational fisheries, 1990s, with a stronger nonnative species Gila River basin to be critically Clarkson et al. (2005, pp. 22–25) influence in the lower reaches where imperiled, cite habitat destruction and propose the designation of entire the northern Mexican gartersnake is nonnative species as the primary factors watersheds as having either native or considered to still occur. Surveys in the for the declines, and call for the control nonnative fisheries and manage for Salt River above Lake Roosevelt indicate and removal of nonnative fish as an these goals aggressively. While some a decline of roundtail chub and other overriding need to prevent the decline discussion within Arizona has taken natives with an increase in flathead and and ultimate extinction of native fish place to designate portions of channel catfish numbers (Voeltz 2002, species within the basin. watersheds as either native or nonnative p. 49). In New Mexico, nonnative fish Northern Mexican gartersnakes can fisheries, the geographic areas under have been identified as the main cause successfully use some nonnative consideration for native fishery for declines observed in roundtail chub species, such as mosquitofish and red development do not currently coincide populations (Voeltz 2002, p. 40). shiner, as prey species. However, all with current populations of northern Douglas et al. (1994, pp. 9–19) provide other nonnative species, most notably Mexican gartersnakes and no immediate
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benefit is provided to the subspecies 1926, as a result of a systematic Arizona in specific regional areas, from their implementation. Clarkson et introduction effort by the State Game drainages, and disassociated wetlands al. (2005, p. 25) suggest that current Department (now, the Arizona Game within or adjacent to the historical management of fisheries within the and Fish Department) for the purposes distribution of the northern Mexican southwestern United States as status of sport hunting and as a food source. gartersnake, including the Kaibab quo will have serious adverse effects to (Tellman 2002, p. 43). Bullfrogs are National Forest (Sredl et al. 1995a, p. 7); native fish species and affect the long- extremely prolific, adept at colonizing the Coconino National Forest (Sredl et term viability of the northern Mexican new areas, and may disperse to al. 1995c, p. 7); the White Mountain gartersnake and to its potential recovery. distances of 6.8 miles (10.9 km) and Apache Reservation (Hulse 1973, p. We are not aware of any studies that likely further within drainages (Bautista 278); Beaver Creek (tributary to the have addressed the direct relationship 2002, p. 131; Rosen and Schwalbe Verde River) (Drost and Nowak 1997, p. between prey base diversity and 2002a, p. 7; Casper and Hendricks 2005, 11); the Watson Woods Riparian northern Mexican gartersnake p. 582). In Arizona, using mark and Preserve near Prescott (Nowak and recruitment and survivorship. However, recapture methods, bullfrogs have been Spille 2001, p. 11); the Tonto National Krause and Burghardt (2001, pp. 100– documented to make overland Forest (Sredl et al. 1995b, p. 9); the 123) discuss the benefits and costs that movements of up to 7 miles (11 Lower Colorado River (Vitt and Ohmart may be associated with diet variability kilometers) across semi-desert grassland 1978, p. 44; Clarkson and DeVos 1986, in the common gartersnake habitat on the Buenos Aires National pp. 42–49; Ohmart et al. 1988, p. 143); (Thamnophis sirtalis), an ecologically Wildlife Refuge (BANWR) (Suhre 2008). the Huachuca Mountains (Rosen and similar species to the northern Mexican Investigators on the BANWR also Schwalbe 1988, Appendix I; Holm and gartersnake. Foraging for mixed-prey observed two bullfrogs at an overland Lowe 1995, pp. 27–35; Sredl et al. 2000, species may impede predator learning, distance of 10 miles (16 kilometers) p. 10; Rosen et al. 2001, Appendix I); as compared to specialization, on a from the nearest source population the Pinaleno Mountains region certain prey species, but may also although the origin of the bullfrogs (Nickerson and Mays 1970, p. 495); the provide long-term benefits (Krause and could not be confirmed. Batista (2002, p. San Bernardino National Wildlife Burghardt 2001, p. 101). Krause and 131) confirmed ‘‘the strong colonizing Refuge (Rosen and Schwalbe 1988, Burghardt (2001, p. 112) stated that skills of the bullfrog and that the Appendix I; 1995, p. 452; 1996, pp. 1– varied predatory experience played an introduction of this exotic species can 3; 1997, p. 1; 2002b, pp. 223–227; important role in the feeding abilities of disturb local anuran communities.’’ gartersnakes through the first 8 months Bullfrogs are voracious, opportunistic, 2002c, pp. 31, 70; Rosen et al. 1995, p. of age. These data suggest that a varied even cannibalistic predators that readily 254; 1996b, pp. 8–9; 2001, Appendix I); prey base might also be important for attempt to consume any animal smaller the Buenos Aires National Wildlife neonatal and juvenile northern Mexican than themselves, including other Refuge (Rosen and Schwalbe 1988, gartersnakes (also a species with a species within the same genus, which Appendix I); the Arivaca Area (Rosen varied diet) and that decreases in the can comprise 80 percent of their diet and Schwalbe 1988, Appendix I; Rosen diversity of the prey base during the (Casper and Hendricks 2005, p. 543). et al. 2001, Appendix I); Cienega Creek young age classes might adversely affect Bullfrogs have a varied diet, which has drainage (Rosen et al. 2001, Appendix the ability of individuals to capture prey been documented to include vegetation, I); Babocamari River drainage (Rosen et throughout their lifespan, in addition to numerous invertebrate and vertebrate al. 2001, Appendix I); Turkey Creek the more obvious effects of reduced prey species which include numerous drainage (Rosen et al. 2001, Appendix availability. species of snakes [eight genera; I); O’Donnell Creek drainage (Rosen et The most conclusive evidence for the including six different species of al. 2001, Appendix I); Appleton- northern Mexican gartersnake’s gartersnakes, two species of Whittell Research Ranch near Elgin intolerance for nonnative fish invasions rattlesnakes, and Sonoran gophersnakes (Rosen et al. 2001, Appendix I); Santa remains the fact that, in most (Pituophis catenifer affinis)] (Bury and Cruz River drainage (Rosen and incidences, nonnative fish species Whelan 1984, p. 5; Clarkson and DeVos Schwalbe 1988, Appendix I; Rosen et al. generally do not occur in the same 1986, p. 45; Holm and Lowe 1995, pp. 2001, Appendix I); San Rafael Valley locations as the northern Mexican 37–38; Carpenter et al. 2002, p. 130; (Rosen et al. 2001, Appendix I); San gartersnake and its native prey species. King et al. 2002; Hovey and Bergen Pedro River drainage (Rosen and Additional information on the decline 2003, pp. 360–361; Casper and Schwalbe 1988, Appendix I; Rosen et al. of the northern Mexican gartersnake’s Hendricks 2005, p. 544; Combs et al. 2001, Appendix I); Bingham Cienega native fish prey species can be found in 2005, p. 439; Wilcox 2005, p. 306; (Rosen et al. 2001, Appendix I); Sulfur Bonar et al. (2004, pp. 4, 79–87); DFT DaSilva et al. 2007, p. 443; Neils and Springs Valley (Rosen et al. 1996a, pp. (2003, pp. 1–3, 5–6, 19; 2004, pp. 1–2, Bugbee 2007, p. 443). 16–17); Whetstone Mountains region 4–5, 10, Table 1; 2006, pp. iii, 25); Bullfrogs have been documented (Turner et al. 1999, p. 11); Aqua Fria Richter et al. (1997, pp. 1081–1093); and throughout the State of Arizona. River drainage (Rosen and Schwalbe Haney et al. (2008, pp. 54–61, 82, 93). Holycross et al. (2006, pp. 13–14, 52– 1988, Appendix I; Holycross et al. 2006, Bullfrog Diet and Distribution. 61) found bullfrogs at 55 percent of pp. 13, 15–18, 52–53); Verde River Bullfrogs are widely considered one of sample sites in the Agua Fria watershed, drainage (Rosen and Schwalbe 1988, the most serious threats to the northern 62 percent of sites in the Verde River Appendix I; Holycross et al. 2006, pp. Mexican gartersnake throughout its watershed, 25 percent of sites in the Salt 13, 26–28, 55–56); greater metropolitan range (Conant 1974, pp. 471, 487–489; River watershed, and 22 percent of sites Phoenix area (Rosen and Schwalbe Rosen and Schwalbe 1988, pp. 28–30; in the Gila River watershed. In total, 1988, Appendix I); greater metropolitan Rosen et al. 2001, pp. 21–22). Bullfrogs bullfrogs were observed at 22 of the 57 Tucson area (Rosen and Schwalbe 1988, adversely affect northern Mexican sites surveyed (39 percent) across the Appendix I); Sonoita Creek drainage gartersnakes through direct predation of Mogollon Rim (Holycross et al. 2006, p. (Rosen and Schwalbe 1988, Appendix juveniles and sub-adults and from 13). A number of authors have also I); Sonoita Grasslands (Rosen and competition with native prey species. documented the presence of bullfrogs Schwalbe 1988, Appendix I); Canelo Bullfrogs first appeared in Arizona in through their survey efforts throughout Hills (Rosen and Schwalbe 1988,
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Appendix I); Pajarito Mountains (pers. pp. 28–30; 2002b, pp. 232–238); Rosen lead to infection or compromise an observation, J. Servoss, Fish and et al. (1995, pp. 257–258; 2001, pp. 2, individual’s physical ability to escape Wildlife Biologist, U.S. Fish and Appendix I); Wu et al. (2005, p. 668); future predation attempts or Wildlife Service); Picacho Reservoir Pearl et al. (2004, p. 18); Kupferberg successfully forage. Tails of gartersnakes (Rosen and Schwalbe 1988, Appendix (1994, p. 95) Kupferburg (1997, pp. do not regenerate. The incidence of tail I); Dry Creek drainage (Holycross et al. 1736–1751); Lawler et al. (1999); Bury breaks in gartersnakes can often be used 2006, pp. 19, 53); Little Ash Creek and Whelan (1986, pp. 9–10); Hayes and to assess predation pressures within drainage (Holycross et al. 2006, pp. 19, Jennings (1986, pp. 500–501); Moyle gartersnake populations. Rosen and 54); Oak Creek drainage (Holycross et al. (1973, pp. 18–22)). Different age classes Schwalbe (1988, p. 22) found the 2006, pp. 23, 54); Sycamore Creek of bullfrogs within a community can incidence of tail breaks to be drainages (Holycross et al. 2006, pp. 20, affect native ranid populations via statistically higher in females than in 25, 54–55); Rye Creek drainage different mechanisms. Juvenile bullfrogs males. Fitch (2003, p. 212) also found (Holycross et al. 2006, pp. 37, 58); affect native ranids through that tail breaks in the common Spring Creek drainage (Holycross et al. competition, male bullfrogs affect native gartersnake occurred more frequently in 2006, pp. 25, 59); Tonto Creek drainage ranids through predation, and female females than males and in adults more (Holycross et al. 2006, pp. 40–44, 59; bullfrogs affect native ranids through than in juveniles. Fitch (2003, p. 212) Wallace et al. 2008, pp. 243–244); San both mechanisms depending on body also commented that, while tail Francisco River drainage (Holycross et size and microhabitat (Wu et al. 2005, breakage in gartersnakes can save the al. 2006, pp. 49–50, 61); Sonoita Creek p. 668). Pearl et al. (2004, p. 18) also life of an individual snake, it also leads (Tuner 2006; p. 10); and the upper Gila suggested that the effect of bullfrog to permanent handicapping of the River drainage (Holycross et al. 2006, introductions on native ranids may be snake, resulting in slower swimming pp. 45–50, 60–61). different based on specific habitat and crawling speeds, which could leave Perhaps one of the most serious conditions, but also suggested that an the snake more vulnerable to predation consequences of bullfrog introductions individual ranid frog species’ physical or affect its foraging ability. is their persistence in an area once they ability to escape influences the effect of Furthermore, Mushinsky and Miller have become established, and the bullfrogs on each native ranid (1993, pp. 662–664) found that the subsequent difficulty in eliminating community. incidence of tail injury in water snakes bullfrog populations. Rosen and Bullfrog Predation on Northern in the genera Nerodia and Regina Schwalbe (1995, p. 452) experimented Mexican Gartersnakes. Sub-adult and (which have similar life histories to with bullfrog removal at various sites on adult bullfrogs not only compete with northern Mexican gartersnakes) was the San Bernardino National Wildlife the northern Mexican gartersnake for higher in females than in males and in Refuge in addition to a control site with prey items, but directly prey upon adults more than juveniles. This can be no bullfrog removal in similar habitat on juvenile and occasionally sub-adult explained by higher basking rates the BANWR. Removal of adult bullfrogs, northern Mexican gartersnakes (Rosen associated with pregnant females that without removal of eggs and tadpoles, and Schwalbe 1988, pp. 28–31; 1995, p. increase their visibility to predators. resulted in a substantial increase in 452; 2002b, pp. 223–227; Holm and Additionally, predation on juvenile younger age-class bullfrogs where Lowe 1995, pp. 29–29; Rossman et al. snakes generally results in complete removal efforts were the most intensive 1996, p. 177; AGFD In Prep, p. 12; 2001, consumption of the animal, which (Rosen and Schwalbe 1997, p. 6). p. 3; Rosen et al. 2001, pp. 10, 21–22; would limit observations of tail injury Contradictory to the goals of bullfrog Carpenter et al. 2002, p. 130; Wallace in their age class. Rosen and Schwalbe eradication, evidence from dissection 2002, p. 116). A well-circulated (1988, p. 22) suggested that the samples from young adult and sub-adult photograph of an adult bullfrog in the indication that female northern Mexican bullfrogs indicated these age-classes process of consuming a northern gartersnakes bear more injuries is readily prey upon juvenile bullfrogs (up Mexican gartersnake at Parker Canyon consistent with the inference that they to the average adult leopard frog size) as Lake, Cochise County, Arizona, taken by employ a riskier foraging strategy. Willis well as juvenile gartersnakes, which John Carr of the Arizona Game and Fish et al. (1982, p. 98) discussed the suggests that the selective removal of Department in 1964, provides incidence of tail injury in three species only the large adult bullfrogs (presumed photographic documentation of bullfrog in the genus Thamnophis (common to be the most dangerous size class to predation (Rosen and Schwalbe 1988, p. leopard frogs and gartersnakes), favoring 29; 1995, p. 452). A common gartersnake, Butler’s gartersnake (T. the young adult and sub-adult age observation in northern Mexican butleri), and the eastern ribbon snake (T. classes, could indirectly lead to gartersnake populations that co-occur sauritus)) and concluded that increased predation of leopard frogs and with bullfrogs is a preponderance of individuals that suffered nonfatal juvenile gartersnakes (Rosen and large, mature adult snakes with injuries prior to reaching a length of 12 Schwalbe 1997, p. 6). These findings conspicuously low numbers of in (30 cm) are not likely to survive and illustrate that in addition to large adults, individuals in the newborn and juvenile that physiological stress during post- bullfrogs in the young adult and age size classes due to bullfrogs preying injury hibernation may play an subadult age classes also negatively on young small snakes, which important role in subsequent mortality. impact northern Mexican gartersnakes ultimately leads to low reproductive Ecologically significant observations and their prey species. rates and survival of young (Rosen and on tail injuries were made by Rosen and Bullfrog Effects on the Native Anuran Schwalbe 1988, p. 18; Holm and Lowe Schwalbe (1988, pp. 28–31) on the Prey Base for the Northern Mexican 1995, p. 34). Potential recruitment formerly occurring population of Gartersnake. As documented above and problems for northern Mexican northern Mexican gartersnakes on the in the following studies, bullfrogs gartersnakes due to effects from San Bernardino National Wildlife significantly reduce native anuran prey nonnative species are also suspected at Refuge. Seventy-eight percent of availability for the northern Mexican Tonto Creek (Wallace et al. 2008, pp. specimens had broken tails with a ‘‘soft gartersnake (Conant (1974, pp. 471, 243–244). and club-like’’ terminus, which suggests 487–489); Hayes and Jennings (1986, pp. The tails of gartersnakes broken off repeated injury from multiple predation 491–492); Rosen and Schwalbe (1988, through predation attempts may also attempts by bullfrogs. While medically
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examining pregnant female northern vertebrate species. Crayfish fed on by northern Mexican gartersnakes, or Mexican gartersnakes, Rosen and embryos, tadpoles, newly sites the investigators believed Schwalbe (1988, p. 28) noted bleeding metamorphosed frogs, and adult leopard possessed suitable habitat and may be from the posterior region which, frogs, but they did not feed on egg occupied based upon the known suggested to the investigators the snakes masses (Fernandez and Rosen 1996, p. historical distribution of the subspecies. suffered from ‘‘squeeze-type’’ injuries 25). However, Gamradt and Kats (1996, Several other authors have inflicted by adult bullfrogs. While a sub- p. 1155) found that crayfish readily specifically documented the presence of adult or adult northern Mexican consumed the egg masses of California crayfish in many areas and drainages gartersnake may survive an individual newts (Taricha torosa). Fernandez and throughout Arizona, which is testament predation attempt from a bullfrog while Rosen (1996, pp. 6–19, 52–56) and to their ubiquitous distribution in only incurring tail damage, secondary Rosen (1987, p. 5) discussed Arizona and their strong colonizing effects from infection of the wound can observations of inverse relationships abilities. These areas all fall within the significantly contribute to mortality of between crayfish abundance and native range of the northern Mexican individuals. reptile and amphibian populations gartersnake and include the Kaibab Research on the effects of attempted including narrow-headed gartersnakes, National Forest (Sredl et al. 1995a, p. 7); predation performed by Mushinsky and northern leopard frogs, and Chiricahua the Coconino National Forest (Sredl et Miller (1993, pp. 661–664) and Willis et leopard frogs. Crayfish may also affect al. 1995c, p. 7); the Watson Woods al. (1982, pp. 100–101) supports the native fish populations. Carpenter Riparian Preserve near Prescott (Nowak observations made by Holm and Lowe (2005, pp. 338–340) documented that and Spille 2001, p. 33); the Tonto (1995, p. 34) on the northern Mexican crayfish may reduce the growth rates of National Forest (Sredl et al. 1995b, p. 9); gartersnake population age class native fish through competition for food the Lower Colorado River (Ohmart et al. structure in Scotia Canyon in the and noted that the significance of this 1988, p. 150; Inman et al. 1998, Huachuca Mountains of southeastern impact may vary between species. Appendix B); the Huachuca Mountains Arizona in the early 1990s. Specifically, Crayfish also prey on fish eggs and (Sredl et al. 2000, p. 10); the Arivaca Holm and Lowe (1995, pp. 33–34) larvae (Inman et al. 1998, p. 17). Area (Rosen et al. 2001, Appendix I); observed a conspicuously greater Crayfish alter the abundance and Babocamari River drainage (Rosen et al. number of adult snakes in that structure of aquatic vegetation by 2001, Appendix I); O’Donnell Creek population than sub-adult snakes, as grazing on aquatic and semiaquatic drainage (Rosen et al. 2001, Appendix well as a higher incidence of tail injury vegetation, which reduces the cover (89 percent) in all snakes captured. needed by frogs and gartersnakes as well I); Santa Cruz River drainage (Rosen and Bullfrogs have been identified as the as the food supply for prey species such Schwalbe 1988, Appendix I; Rosen et al. primary cause for both the collapse of as tadpoles (Fernandez and Rosen 1996, 2001, Appendix I); San Pedro River the native leopard frog (prey base for the pp. 10–12). Fernandez and Rosen (1996, drainage (Inman et al. 1998, Appendix northern Mexican gartersnake) and pp. 10–12) also found that crayfish B; Rosen et al. 2001, Appendix I); Aqua northern Mexican gartersnake frequently burrow into stream banks, Fria River drainage (Inman et al. 1998, populations on the San Bernardino which leads to increased bank erosion, Appendix B; Holycross et al. 2006, pp. National Wildlife Refuge (Rosen and stream turbidity, and siltation of 14, 15–18, 52–54); Verde River drainage Schwalbe 1988, p. 28; 1995, p. 452; substrates. Creed (1994, p. 2098) found (Inman et al. 1998, Appendix B; 1996, pp. 1–3; 1997, p. 1; 2002b, pp. that filamentous alga (Cladophora Holycross et al. 2006, pp. 14, 20–28, 54– 223–227; 2002c, pp. 31, 70; Rosen et al. glomerata) was at least 10-fold greater in 56); Salt River drainage (Inman et al. 1996b, pp. 8–9). Rosen and Schwalbe aquatic habitat absent crayfish. 1998, Appendix B; Holycross et al. (1988, p. 18) stated that the low Filamentous alga is an important 2006, pp. 15, 29–44, 56–60); Black River survivorship of newborns, and possibly component of aquatic vegetation that drainage (Inman et al. 1998, Appendix yearlings, due to bullfrog predation is an provides cover for foraging gartersnakes B); San Francisco River drainage (Inman important proximate cause of as well as microhabitat for prey species. et al. 1998, Appendix B; Holycross et al. population declines of this snake at the Inman et al. (1998, p. 3) documented 2006, pp. 14, 49–50, 61); Nutrioso Creek San Bernardino National Wildlife nonnative crayfish as widely distributed drainage (Inman et al. 1998, Appendix Refuge and throughout its distribution and locally abundant in a broad array of B); Little Colorado River drainage in Arizona. natural and artificial free-flowing and (Inman et al. 1998, Appendix B); Crayfish. Nonnative crayfish are a still-water habitats throughout Arizona, Leonard Canyon Drainage (Inman et al. primary threat to many prey species of many of which overlapped the historical 1998, Appendix B); East Clear Creek the northern Mexican gartersnake and and current distribution of the northern drainage (Inman et al. 1998, Appendix may also prey upon juvenile Mexican gartersnake. Hyatt (undated, p. B); Chevelon Creek drainage (Inman et gartersnakes (Fernandez and Rosen 71) concluded that the majority of al. 1998, Appendix B); Eagle Creek 1996, p. 25; Voeltz 2002, pp. 87–88; waters in Arizona contained at least one drainage (Inman et al. 1998, Appendix USFWS 2007, p. 22). Fernandez and species of crayfish. In surveying for B; Holycross et al. 2006, pp. 47–48, 60); Rosen (1996, p. 3) studied the effects of northern Mexican and narrow-headed Bill Williams drainage (Inman et al. crayfish introductions on two stream gartersnakes, Holycross et al. (2006, p. 1998, Appendix B); Sabino Canyon communities in Arizona, a low- 14) found crayfish in 64 percent of the drainage (Inman et al. 1998, Appendix elevation semi-desert stream and a high sample sites in the Agua Fria watershed; B); Dry Creek drainage (Holycross et al. mountain stream, and concluded that in 85 percent of the sites in the Verde 2006, pp. 19, 53); Little Ash Creek crayfish can noticeably reduce species River watershed; in 46 percent of the drainage (Holycross et al. 2006, pp. 19, diversity and destabilize food chains in sites in the Salt River watershed; and in 54); Sycamore Creek drainage riparian and aquatic ecosystems through 67 percent of the sites in the Gila River (Holycross et al. 2006, pp. 25, 54–55); their effect on vegetative structure, watershed. In total, crayfish were East Verde River drainage (Holycross et stream substrate (stream bottom; i.e., observed at 35 (61 percent) of the 57 al. 2006, pp. 21–22, 54); Oak Creek silt, sand, cobble, boulder) composition, sites surveyed across the Mogollon Rim drainage (Holycross et al. 2006, pp. 23, and predation on eggs, larval, and adult (Holycross et al. 2006, p. 14), most of 54); Pine Creek drainage (Holycross et forms of native invertebrate and which were sites historically occupied al. 2006, pp. 24, 55); Spring Creek
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drainage (Holycross et al. 2006, pp. 25, Blue River drainage; the Campbell Blue fins of these species can become lodged 55); Big Bonito Creek drainage River drainage; the Eagle Creek in, or cut into the gut tissue, of the (Holycross et al. 2006, pp. 29, 56); drainage; and the San Francisco River snake, as observed in narrow-headed Cherry Creek drainage (Holycross et al. drainage. Other authors have gartersnakes (Nowak and Santana- 2006, pp. 33, 57); East Fork Black River documented the presence of nonnative Bendix 2002, p. 25). drainage (Holycross et al. 2006, pp. 34, fish through their survey efforts in Nonnative fish invasions can 57); Haigler Creek drainage (Holycross specific regions that include the Tonto indirectly affect the health, et al. 2006, pp. 35, 58); Houston Creek National Forest (Sredl et al. 1995b, p. 8) maintenance, and reproduction of the drainage (Holycross et al. 2006, pp. 35– and the Huachuca Mountains (Sredl et northern Mexican gartersnake by 36, 58); Rye Creek drainage (Holycross al. 2000, p. 10). altering its foraging strategy and et al. 2006, pp. 37, 58); Tonto Creek Holycross et al. (2006, pp. 14–15) foraging success. The more energy drainage (Holycross et al. 2006, pp. 40– found nonnative fish species in 64 expended in foraging, coupled by the 44, 59; Wallace et al. 2008; pp. 243– percent of the sample sites in the Agua reduced number of small to medium- 244); Blue River drainage (Holycross et Fria watershed, 85 percent of the sample sized prey fish available in lower al. 2006, pp. 45, 60); Campbell Blue sites in the Verde River watershed, 75 densities, may lead to deficiencies in River drainage (Holycross et al. 2006, percent of the sample sites in the Salt nutrition affecting growth and pp. 46, 60); and the Gila River drainage River watershed, and 56 percent of the reproduction because energy is instead (Inman et al. 1998, Appendix B; sample sites in the Gila River allocated to maintenance and the Holycross et al. 2006, pp. 45–50, 61). watershed. In total, nonnative fish were increased energy costs of intense Like bullfrogs, crayfish can be very observed at 41 of the 57 sites surveyed foraging activity (Rosen et al. 2001, p. difficult, if not impossible, to eradicate (72 percent) across the Mogollon Rim 19). In contrast, a northern Mexican once they have become established in (Holycross et al. 2006, p. 14). Entirely gartersnake diet that includes both fish an area (Rosen and Schwalbe 1996a, pp. native fish communities were detected and amphibians such as leopard frogs 5–8; 2002a, p. 7; Hyatt undated, pp. 63– in only 8 of 57 sites surveyed (14 provides larger prey items which reduce 71). percent) (Holycross et al. 2006, p. 14). the necessity to forage at a higher While the locations and drainages frequency allowing metabolic energy Nonnative Fish Distribution and identified above that are known to gained from larger prey items to be Community Interactions. As indicated support populations of nonnative fish allocated instead to growth and earlier in this document, nonnative fish do not provide a thorough reproductive development. Myer and are a threat to northern Mexican representation of the status of nonnative Kowell (1973, p. 225) experimented gartersnakes and their native anuran fish distribution Statewide in Arizona, it with food deprivation in common and fish prey. Similar to bullfrogs, is well documented that nonnative fish gartersnakes and found significant predatory nonnative fish species, such have infiltrated the majority of aquatic reductions in lengths and weights in as largemouth bass, also prey upon communities in Arizona. juvenile snakes that were deprived of juvenile northern Mexican gartersnakes. Nonnative fish can also affect native regular feedings versus the control Rosen et al. (2001, Appendix I) and amphibian populations. Matthews et al. group that were fed regularly at natural Holycross et al. (2006, pp. 15–51) (2002, p. 16) examined the relationship frequencies. Reduced foraging success conducted large-scale surveys for of gartersnake distributions, amphibian means that individuals will become northern Mexican gartersnakes in population declines, and nonnative fish vulnerable to effects from starvation, southeastern and central Arizona and introductions in high-elevation aquatic which may, therefore, increase mortality narrow-headed gartersnakes in central ecosystems in California. Matthews et rates in the juvenile size class and and east-central Arizona and al. (2002, p. 16) specifically examined consequently affect recruitment of documented the presence of nonnative the effect of nonnative trout northern Mexican gartersnakes where fish at many locations. Rosen et al. introductions on populations of their prey base has been compromised (2001, Appendix I) found nonnative fish amphibians and mountain gartersnakes by nonnative species. in the following survey locations: The (Thamnophis elegans elegans). Their Nonnative Species in Mexico. As in Arivaca Area; Babocamari River results indicated the probability of the United States, the native fish prey drainage; O’Donnell Creek drainage; observing gartersnakes was 30 times base for northern Mexican gartersnakes Appleton-Whittell Research Ranch (Post greater in lakes containing amphibians in Mexico has been dramatically Canyon) near Elgin; Santa Cruz River than in lakes where amphibians have affected by the introduction of drainage; Agua Caliente Canyon; Santa been extirpated by nonnative fish. These nonnative species (Conant 1974, pp. Catalina Mountains; and the San Pedro results supported prediction by Jennings 471, 487–489; Miller et al. 2005, pp. 60– River drainage. Holycross et al. (2006, et al. (1992, p. 503) that native 61; Abarca 2006). In the lower pp. 14–15, 52–61) found nonnative fish amphibian declines will lead directly to elevations of Mexico where northern in the Aqua Fria River drainage; the gartersnake declines. Matthews et al. Mexican gartersnakes occurred Verde River drainage; the Dry Creek (2002, p. 20) noted that in addition to historically or are still found, there are drainage; the Little Ash Creek drainage; nonnative fish species adversely approximately 200 species of native the Sycamore Creek drainage; the East impacting amphibian populations that freshwater fish documented with 120 Verde River drainage; the Oak Creek are part of the gartersnake’s prey base, native species under some form of threat drainage; the Pine Creek drainage; the direct predation on gartersnakes by and an additional 15 that have become Big Bonito Creek drainage; the Black nonnative fish also occurs. Inversely, extinct due to human activities, which River drainage; the Canyon Creek gartersnake predation on nonnative include the introduction of nonnative drainage; the Cherry Creek drainage; the species, such as centrarchids, may species (Contreras Balderas and Lozano Christopher Creek drainage; the East physically harm the snake. Choking 1994, pp. 383–384). In 1979, The Fork Black River drainage; the Haigler injuries to northern Mexican American Fisheries Society listed 69 Creek drainage; the Houston Creek gartersnakes may occur from attempting species of native fish in Mexico as drainage; the Rye Creek drainage; the to ingest nonnative spiny-rayed fish threatened or in danger of becoming Salt River drainage; the Spring Creek species (such as green sunfish and bass) extinct. Ten years later that number rose drainage; the Tonto Creek drainage; the because the spines located in the dorsal to 123 species, an increase of 78 percent
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(Contreras Balderas and Lozano 1994, available for purchase at Mexican pet threat to northern Mexican gartersnakes, pp. 383–384). Miller et al. (2005, p. 60) stores (Luja and Rodrı´guez-Estrella Bd does have a widespread effect on concludes that some 20 percent of 2008, p. 22). anuran prey availability for the species. Mexico’s native fish are threatened or in Adverse effects such as predation In addition, stress placed on northern danger of becoming extinct. Nonnative upon, and competition with, northern Mexican gartersnakes as a result of species are increasing everywhere Mexican gartersnakes and their prey threats discussed under Factor A may throughout Mexico, and this trend will base from bullfrog invasions in Mexico affect the health condition of have adverse impacts on native fish, have been specifically documented with individuals within populations affected according to Miller et al. (2005, p. 61). respect to Chiricahua leopard frogs, a by these threats, which may increase the A number of freshwater fish populations primary prey item for northern Mexican potential for disease within current have been adversely affected by gartersnakes (Luja and Rodrı´guez- populations in the future. nonnative species in many locations, Estrella 2008, p. 21). Luja and Direct predation by nonnative several of which were previously noted Rodrı´guez-Estrella (2008, p. 21) also bullfrogs, crayfish, and fishes on in the discussion under Factor A. stated that bullfrog eradication efforts in northern Mexican garter snakes is a At the time of our 2006 12-month Mexico are often thwarted by their being significant threat rangewide, as is finding, we had less information on the favored by local communities. predation on gartersnake prey species status and distribution of bullfrogs Currently, no regulation exists in (competition) by these same groups of within Mexico. However, since that Mexico to address the threat of bullfrog nonnative taxa. Nonnative fish, crayfish, time, Luja and Rodrı´guez-Estrella (2008, invasions (Luja and Rodrı´guez-Estrella and bullfrogs have reduced native pp 17–22) examined the invasion of the 2008, p. 22). populations of prey species throughout bullfrog in Mexico. The earliest records Rosen and Melendez (2006, p. 54) the range. of bullfrogs in Mexico were Nuevo Leon report bullfrog invasions to be prevalent D. The Inadequacy of Existing (1853), Tamaulipas (1898), Morelos in northwestern Chihuahua and Regulatory Mechanisms (1968), and Sinaloa (1969) (Luja and northwestern Sonora, where the Rodrı´guez-Estrella 2008, p 20). By 1976, northern Mexican gartersnake is thought Currently, the northern Mexican the bullfrog was documented in 7 more to occur. In many areas, native leopard gartersnake is considered ‘‘State States: Aguacalientes, Baja California frogs were completely displaced where Endangered’’ in New Mexico. In the Sur, Chihuahua, Distrito Federal, bullfrogs were observed. Rosen and State of New Mexico, an ‘‘Endangered Puebla, San Luis Potosi, and Sonora Melendez (2006, p. 54) also Species’’ is defined as ‘‘any species of (Luja and Rodrı´guez-Estrella 2008, p. demonstrated the relationship between fish or wildlife whose prospects of 20). To date, Luja and Rodrı´guez- fish and amphibian communities in survival or recruitment within the State Estrella (2008, p. 20) have recorded Sonora and western Chihuahua. Native are in jeopardy due to any of the bullfrogs in 20 of the 31 Mexican States leopard frogs, a primary prey item for following factors: (1) The present or (65 percent of the states in Mexico) and the northern Mexican gartersnake, only threatened destruction, modification, or suspect that they have invaded other occurred in the absence of nonnative curtailment of its habitat; (2) States, but were unable to find fish and were absent from waters overutilization for scientific, documentation. containing nonnative species, which commercial or sporting purposes; (3) the Sponsored by the then Mexican included several major waters. In effect of disease or predation; (4) other Secretary of Aquaculture Support, Sonora, Rorabaugh (2008, p. 25) also natural or man-made factors affecting its bullfrogs have been commercially considers the bullfrog to be a significant prospects of survival or recruitment produced for food in Mexico in threat to the northern Mexican within the state; or (5) any combination Yucatan, Nayarit, Morelos, Estado de gartersnake and its prey base. of the foregoing factors’’ as per New Mexico, Michoaca´n, Guadalajara, San Unmack and Fagan (2004, p. 233) Mexico Statutory Authority (NMSA) 17– Luis Potosi, Tamaulipas, and Sonora compared historical museum collections 2–38.D. ‘‘Take,’’ defined as ‘‘means to (Luja and Rodrı´guez-Estrella 2008, p. of nonnative fish species from the Gila harass, hunt, capture or kill any wildlife 20). However, frog legs ultimately never River basin in Arizona and the Yaqui or attempt to do so’’ by NMSA 17–2– gained popularity in Mexican culinary River basin in Sonora, Mexico, to gain 38.L., is prohibited without a scientific culture (Conant 1974, pp. 487–489) and insight into the trends in distribution, collecting permit issued by the New Luja and Rodrı´guez-Estrella (2008, p. diversity, and abundance of nonnative Mexico Department of Game and Fish as 22) point out that only 10 percent of fishes in each basin over time. They per NMSA 17–2–41.C and New Mexico these farms remain in production. Luja found that nonnative species are slowly Administrative Code (NMAC) 19.33.6. and Rodrı´guez-Estrella (2008, p. 20 and but steadily increasing in all three However, while the New Mexico 22) document instances where bullfrogs parameters in the Yaqui Basin (Unmack Department of Game and Fish can issue have escaped production farms and and Fagan 2004, p. 233). Unmack and monetary penalties for illegal take of suspect the majority of the frogs that Fagan (2004, p. 233) predicted that, in northern Mexican gartersnakes, the were produced commercially in farms the absence of aggressive management same provisions are not in place for that have since ceased operation have intervention, significant extirpations or actions that result in loss or assimilated into surrounding habitat. range reductions of native fish species modification of habitat (NMSA 17–2– Luja and Rodrı´guez-Estrella (2008, p. are expected to occur in the Yaqui Basin 41.C and NMAC 19.33.6) (Painter 2005). 20) also state that Mexican people of Sonora, Mexico, which may have The northern Mexican gartersnake is deliberately introduce bullfrogs for current populations of northern considered a ‘‘Candidate Species’’ in the ornamental purposes, or ‘‘for the simple Mexican gartersnake, as did much of the Arizona Game and Fish Department pleasure of having them in ponds.’’ The Gila Basin before the introduction of draft document, Wildlife of Special act of deliberately releasing bullfrogs nonnative species. Loss of native fishes Concern (WSCA) (AGFD In Prep., p. 12). into the wild in Mexico was cited by will impact prey availability for the A ‘‘Candidate Species’’ is one ‘‘whose Luja and Rodrı´guez-Estrella (2008, p. northern Mexican gartersnake and threats are known or suspected but for 21) as being ‘‘more common than we threaten its persistence in these areas. which substantial population declines can imagine.’’ To further compound Summary of Factor C. While disease from historical levels have not been these introductions, bullfrogs are is not currently considered a direct documented (though they appear to
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have occurred)’’ (AGFD In Prep., p. 12). purposes or for other reasons. These (the Mexican equivalent to a threatened The purpose of the WSCA list is to encounters can result in the capture, and endangered species list), and if provide guidance in habitat injury, or death of the gartersnake due appropriate, the nomination of species management implemented by land- to the lay person’s fear or dislike of to the list. INE is generally considered management agencies. Additionally, the snakes (Rosen and Schwalbe 1988, p. the Mexican counterpart to the United northern Mexican gartersnake is 43; Ernst and Zug 1996, p. 75; Green States’ Fish and Wildlife Service. INE considered a ‘‘Tier 1b Species of 1997, pp. 285–286; Nowak and Santana- developed the Method of Evaluation of Greatest Conservation Need’’ in the Bendix 2002, p. 39). It is very difficult the Risk of Extinction of the Wild Arizona Game and Fish Department for the Arizona Game and Fish Species in Mexico (MER), which unifies draft document, Arizona’s Department or the New Mexico the criteria of decisions on the Comprehensive Wildlife Conservation Department of Fish and Game to categories of risk and permits the use of Strategy (CWCS) (AGFD 2006a, p. 32; monitor or even be aware of such forms specific information fundamental to 2006b). The purpose for the CWCS is to of take. We believe that unregulated take listing decisions. The MER is based on ‘‘provide an essential foundation for the occurs, particularly in areas frequently four independent, quantitative criteria: future of wildlife conservation and a visited by the public with current (1) Size of the distribution of the taxon stimulus to engage the States, federal populations of northern Mexican in Mexico; (2) state (quality) of the agencies, and other conservation gartersnakes, such as at Page Springs habitat with respect to natural partners to strategically think about and Bubbling Ponds hatcheries and development of the taxon; (3) intrinsic their individual and coordinated roles along Tonto Creek near the town of biological vulnerability of the taxon; in prioritizing conservation efforts’’ Gisela. We are reasonably certain that and (4) impacts of human activity on the (AGFD 2006a, p. 2). A ‘‘Tier 1b Species the level of illegal field collecting by the taxon. INE began to use the MER in of Greatest Conservation Need’’ is one hobbyist community is low because 2006; therefore, all species previously that requires immediate conservation gartersnakes are relatively undesirable listed in the NOM–059 were based actions aimed at improving conditions in amateur herpetological collections. solely on expert review and opinion in through intervention at the population Neither the New Mexico Department many cases. Specifically, until 2006, the or habitat level (AGFD 2006a, p. 32). of Game and Fish, nor the Arizona listing process under INE consisted of a Prior to 2005, the Arizona Game and Game and Fish Department have panel of scientific experts who Fish Department allowed for take of up specified or mandated recovery goals for convened as necessary for the purpose to four northern Mexican gartersnakes the northern Mexican gartersnake, nor of defining and assessing the status and per person per year as specified in has either State developed a threats that affect Mexico’s native Commission Order Number 43. The conservation agreement or plan for this species that are considered to be at risk Arizona Game and Fish Department species. and applying those factors to the defines ‘‘take’’ as ‘‘pursuing, shooting, Throughout Mexico, the Mexican definitions of the various listing hunting, fishing, trapping, killing, gartersnake is listed at the species level categories. In 1994, when the Mexican capturing, snaring, or netting wildlife or of its taxonomy as ‘‘Amenazadas,’’ or gartersnake was placed on the NOM– the placing or using any net or other Threatened, by the Secretaria de Medio 059 (SEDESOL 1994 (NOM–059–ECOL– device or trap in a manner that may Ambiente y Recursos Naturales 1994), p. 46) as a threatened species, the result in the capturing or killing of (SEMARNAT) (SEDESOL 2001). decision was made by a panel of wildlife.’’ The Arizona Game and Fish Threatened species are ‘‘those species, scientific experts. Department subsequently amended or populations of the same, likely to be Although the Mexican gartersnake is Commission Order Number 43, effective in danger of disappearing in a short or considered a federally threatened January 2005. Take of northern Mexican medium timeframe, if the factors that species in Mexico, no recovery plan or gartersnakes is no longer permitted in negatively impact their viability, cause other conservation planning occurs Arizona without issuance of a scientific the deterioration or modification of their because of this status. Enforcement of collecting permit (Ariz. Admin. Code habitat or directly diminish the size of the regulation protecting the gartersnake R12–4–401 et seq.). While the Arizona their populations continue to operate’’ is sporadic, based on available resources Game and Fish Department can seek (SEDESOL 2001 (NOM–059–ECOL– and location. Based upon the criminal or civil penalties for illegal 2001), p. 4). This designation prohibits information on the status of the species take of northern Mexican gartersnakes, taking of the species, unless specifically and the historic and continuing threats the same provisions are not in place for permitted, as well as prohibits any to its habitat in Mexico, our analysis actions that result in destruction or activity that intentionally destroys or concludes that protections afforded to modification of northern Mexican adversely modifies its habitat (SEDESOL the northern Mexican gartersnake may gartersnake habitat. 2000 (LGVS) and 2001 (NOM–059– not be adequate to preclude the In addition to making the necessary ECOL–2001)). Additionally, in 1988, the continued decline of this species regulatory changes to promote the Mexican Government passed a throughout its range. conservation of the northern Mexican regulation that is similar to the National Ortega-Huerta and Kral (2007, p. 1) gartersnake, the Arizona Game and Fish Environmental Policy Act of the United found that land legislation within Department continues as a strong States (42 U.S.C. 4321 et seq.). This Mexico has changed considerably over partner in research and survey efforts Mexican regulation requires an recent years to integrate free market that further our understanding of environmental assessment of private or policies into local agricultural current populations within Arizona. government actions that may affect production methods. This may result in They continue to assist with future wildlife or their habitat (SEDESOL 1988 the loss of land management practices conservation efforts and the (LGEEPA)). that protect the natural environment. In establishment of long-term conservation The Mexican Federal agency known 1992, the Mexican Government made a partnerships. as the Instituto Nacional de Ecologı´a constitutional amendment ending the Gartersnakes are active, diurnal (INE) is responsible for the analysis of Ejido’s special legal status and (daytime) foragers and humans the status and threats that pertain to permitting the sale of collectively encounter gartersnake species in species that are proposed for listing in controlled lands (Ortega-Huerta and riparian areas used for recreational the Norma Oficial Mexicana NOM–059 Kral 2007, p. 2). An Ejido is an
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amalgamation of various types of management decisions. Individual U.S. northern Mexican gartersnake address ownership of a particular piece of land, Forest Service biologists who work the direct take of individuals without a e.g., state, cooperative, communal, and within the range of the northern permit, and unpermitted take by private. Ejidos are generally managed in Mexican gartersnake may recreationists or collectors is not traditional means, which generally have opportunistically gather data for their thought to be at levels that impact the less of an impact to the environment records on gartersnakes observed subspecies. Arizona and New Mexico compared to more modern free market incidentally in the field, although it is statutes do not provide protection of uses, resulting in higher levels of not required. habitat and ecosystems. Legislation in biodiversity (Ortega-Huerta and Kral Activities that could adversely affect Mexico prohibits intentional destruction 2007, p. 2; Randall 1996, pp. 218–220; northern Mexican gartersnakes and their or modification of the snake’s habitat, Kiernan 2000, pp. 13–23). The loss of habitat continue to occur throughout but neither that or prohibitions on take regulation that prevented the division their current distribution on National appear to be adequate to preclude the and sale of collectively controlled lands Forest lands. Clary and Webster (1989, continued decline of the subspecies. in Mexico is likely to reduce the p. 1) stated that ‘‘* * * most riparian Currently, there are no regulatory protection of intact northern Mexican grazing results suggest that the specific mechanisms in place that specifically gartersnake habitat. grazing system used is not of dominant target the conservation of northern Existing water laws in Arizona, New importance, but good management is— Mexican gartersnake habitat. Legislation Mexico, and Mexico are inadequate to with control of use in the riparian area in Mexico has removed regulation of protect wildlife. The presence of water a key item.’’ Due to ongoing constraints ejidos that promoted intact protection of is a primary habitat constituent for the in funding, staff levels, and time and important riparian and aquatic habitats. northern Mexican gartersnake. Gelt regulatory compliance pertaining to Regulations protecting the quantity and (2008, pp. 1–12) highlighted the fact monitoring and reporting duties tied to quality of water in riparian and aquatic that, because the existing water laws are land management, proactive measures communities are inadequate to protect so old, they reflect a legislative continue to be limited. These factors water resources for the northern interpretation of the resource that is not affect a land manager’s ability to employ Mexican gartersnake, particularly in the consistent with what we know today; adaptive management procedures when face of the significant population growth yet the laws have never been updated or effects to sensitive species or their expected within the historical range of amended to account for this habitat could be occurring at levels the snake discussed under Factor A. discrepancy. For example, over 100 greater than anticipated in regulatory years ago when Arizona’s water laws compliance mechanisms, such as in E. Other Natural or Manmade Factors were written, the important connection section 7 consultation under the Act for Affecting Its Continued Existence between groundwater and surface water listed species that may co-occur with Competition With Other Species was not known (Gelt 2008, pp. 1–12). the northern Mexican gartersnake in an Within the Same Genus. Marcy’s Gelt (2008, pp. 8–9) suggested that area. In other words, and due to the checkered gartersnake (Thamnophis preserving stream flows and riparian existing regulatory framework, some marcianus marcianus) may impact the areas may be better accomplished by land managers may not have the future conservation of the northern curtailing surface water uses rather than flexibility required to adopt adaptive Mexican gartersnake in southern ground water uses, and that the prior management where necessary to Arizona, although supporting data are appropriation doctrine (appropriation of adequately account for adverse effects of limited. Marcy’s checkered gartersnake water rights based upon the water law projects on public lands. is a semi-terrestrial species that is able concept of ‘‘first in use, first in rights’’) Riparian communities are complex to co-exist to some degree with riparian may be outdated and impractical for and recognized as unique in the and aquatic nonnative predators. This is arid areas like Arizona. southwestern United States but are largely due to its ability to forage in The majority of current populations of highly sensitive to many human-caused more terrestrial habitats, specifically in northern Mexican gartersnake in the land uses, as evidenced by the the juvenile size classes (Rosen and United States occur on lands managed comparatively high number of federally Schwalbe 1988, p. 31; Rosen et al. 2001, by the U.S. Bureau of Land Management listed riparian or aquatic species. Four pp. 9–10). In every age class, the and U.S. Forest Service. Although both primary prey species for the northern northern Mexican gartersnake forages in agencies have riparian protection goals, Mexican gartersnake, the Chiricahua aquatic habitats where bullfrogs, neither agency has specific management leopard frog, Gila topminnow, Gila nonnative sportfish, and crayfish also plans for the northern Mexican chub, and roundtail chub, are federally occur, which increases not only the gartersnake. The U.S. Bureau of Land listed or were petitioned for listing. encounter rate between the species but Management considers the northern Other listed or proposed riparian also the juvenile mortality rate of the Mexican gartersnake as a ‘‘Special species or their proposed or designated northern Mexican gartersnake. As Status Species,’’ and agency biologists critical habitat overlap the current or northern Mexican gartersnake numbers actively attempt to identify gartersnakes historical distribution of the northern decline within a population, space observed incidentally during fieldwork Mexican gartersnake. Despite secondary becomes available for occupation by for their records (Young 2005). protections that may be afforded to the checkered gartersnakes. Marcy’s Otherwise, no specific protection or northern Mexican gartersnake from checkered gartersnake subsequently land-management consideration is federally listed species or their critical affects the maximum number of afforded to the species on Bureau of habitat, riparian and aquatic northern Mexican gartersnakes that an Land Management lands. communities continue to be adversely area can maintain based upon available The U.S. Forest Service does not impacted for reasons previously resources and could potentially include northern Mexican gartersnake discussed, contributing to the declining accelerate the decline of or preclude on their Management Indicator Species status of the northern Mexican reoccupancy by the northern Mexican List, but it is included on the Regional gartersnake throughout its range in the gartersnake (Rosen and Schwalbe 1988, Forester’s Sensitive Species List. This United States. p. 31). means that northern Mexican Summary of Factor D. Existing Rosen et al. (2001, pp. 9–10) gartersnakes are considered in land regulations within the range of the documented the occurrence of Marcy’s
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checkered gartersnakes out-competing Changes to climatic patterns are percent, and 33.3 percent, respectively and replacing northern Mexican predicted to have implications for the (Eaton and Scheller 1996, p. 1,111). gartersnakes at the San Bernardino effect of, and management for, Rahel and Olden (2008, p. 526) expect National Refuge and surrounding nonnative species within the that increases in water temperatures in habitats of the Black Draw. They distribution of the northern Mexican drier climates such as the southwestern suspected that the drought from the late gartersnake. Based upon climate change United States will result in periods of 1980s through the late 1990s played a models, nonnative species biology, and prolonged low flows and stream drying. role in the degree of competition for ecological observations, Rahel et al. These effects from changing climatic aquatic resources, provided an (2008, p. 551) conclude that climate conditions may have profound effects advantage to the more versatile Marcy’s change could foster the expansion of on the amount, permanency, and quality checkered gartersnake, and expedited nonnative aquatic species into new of habitat for the northern Mexican the decline of the northern Mexican areas, magnify the effects of existing gartersnake and its prey base. gartersnake. The competition between aquatic nonnative species where they Warmwater nonnative species such as these two species, in combination with currently occur, increase nonnative red shiner, common carp, mosquitofish, other factors described above that have predation rates, and heighten the and largemouth bass are expected to adversely affected the northern Mexican virulence of disease outbreaks in North benefit from prolonged periods of low gartersnake prey base and the suitability America. Many of the nonnative species flow (Rahel and Olden 2008, p. 527). of occupied and formerly occupied have similar, basic ecological Data specific to changing climatic habitat, may be contributing to the requirements as our native species, such patterns in Mexico, other than the decline of this species. as the need for permanent or nearly Seager et al. (2007) climate change modeling, are limited. However, Current and Future Effects from permanent water. Therefore, it is likely that effects from changes to climatic because the predictive climate models Changes in Climatic Patterns and include northern Mexico, we assume Drought. Seagar et al. (2007, pp. 1181– patterns (such as a trend towards a more arid environment) that negatively affect that the changes predicted for the 1184) analyzed 19 different computer southwestern United States will likely models of differing variables to estimate nonnative species such as bullfrogs and nonnative fish may also negatively be similar. the future climatology of the The effects of the water withdrawals affect native prey species for the southwestern United States and discussed above may be exacerbated by northern Mexican gartersnake. northern Mexico in response to the current, long-term drought facing predictions of changing climatic Changes to climatic patterns may the arid southwestern United States. patterns. All but 1 of the 19 models warm water temperatures, alter stream Philips and Thomas (2005, pp. 1–4) predicted a drying trend within the flow events, and may increase demand provided streamflow records that Southwest; one predicted a trend for water storage and conveyance indicate that the drought Arizona toward a wetter climate (Seager et al. systems (Rahel and Olden 2008, pp. experienced between 1999 and 2004 2007, p. 1181). A total of 49 projections 521–522). Warmer water temperatures was the worst drought since the early were created using the 19 models and across temperate regions are predicted 1940s and possibly earlier. The Arizona all but 3 predicted a shift to increasing to expand the distribution of existing Drought Preparedness Plan Monitoring aridity (dryness) in the Southwest as aquatic nonnative species by providing Technical Committee (ADPPMTC) early as 2021–2040 (Seager, et al. 2007, 31 percent more suitable habitat for (2008) assessed Arizona’s drought status p. 1181). The northern Mexican aquatic nonnative species, which are through June 2008 in watersheds where gartersnake and its prey base depend on often tropical in origin and adaptable to the northern Mexican gartersnake permanent or nearly permanent water warmer water temperatures. This occurs or historically occurred. They for survival. A large percentage of conclusion is based upon studies that found that the Verde, Agua Fria, San habitat within the current distribution compared the thermal tolerances of 57 Pedro, Santa Cruz, and Whitewater of the northern Mexican gartersnake is fish species with predictions made from Draw watersheds continue to experience predicted to be at risk of becoming more climate change temperature models moderate drought (ADPPMTC 2008). arid (Seager et al. 2007, pp. 1183–1184), (Mohseni et al. 2003, p. 389). Eaton and Whereas the Salt, Upper Gila, Lower which has severe implications to the Scheller (1996, p. 1,111) reported that Gila, and Lower Colorado watersheds integrity of aquatic and riparian while several cold-water fish species in were abnormally dry (ADPPMTC 2008). ecosystems and the water that supports North America are expected to have Ongoing drought conditions have them. Potential drought associated with reductions in their distribution from depleted recharge of aquifers and changing climatic patterns may not only effects of climate change, several decreased baseflows in the region. adversely affect habitat of the northern warmwater fish species are expected to While drought periods have been Mexican gartersnake, but also its prey. increase their distribution. In the relatively numerous in the arid Amphibians may be among the first southwestern United States, this Southwest from the mid-1800s to the vertebrates to exhibit broad-scale situation may occur where the quantity present, the effects of human-caused changes in response to changes in global of water is sufficient to sustain effects of impacts on riparian and aquatic climatic patters due to their sensitivity potential prolonged drought conditions communities have compromised the to changes in moisture and temperature but where water temperature may warm ability of these communities to function (Reaser and Blaustein 2005, p. 61). to a level found suitable to harmful under the additional stress of prolonged Changes in temperature and moisture, nonnative species that were previously drought conditions. Holycross et al. combined with the ongoing threat to physiologically precluded from (2006, pp. 52–53) recently documented amphibians from the persistence of Bd occupation of these areas. Species that the effects of drought on northern may cause prey species to experience are particularly harmful to northern Mexican gartersnake habitat in the increased physiological stress and Mexican gartersnake populations such vicinity of Arcosante along the Agua decreased immune system function, as the green sunfish, channel catfish, Fria River and at Big Bug Creek. The possibly leading to disease outbreaks largemouth bass, and bluegill are streams were completely dry and (Carey and Alexander 2003, pp. 111– expected to increase their distribution therefore unsuitable northern Mexican 121; Pounds et al. 2006, pp. 161–167). by 7.4 percent, 25.2 percent, 30.4 gartersnake habitats.
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Summary of Factor E. It is unlikely knowledge of the threats to and status resulted in significant declines in native that competition with other gartersnakes of the northern Mexican gartersnake in fish and ranid frog distribution and will be a significant cause of decline in Mexico is not as robust as that for the abundance, and the subsequent listing northern Mexican gartersnake United States, our analysis focuses on of 19 of Arizona’s 31 native fish species populations in comparison to other the United States and presumes (1) throughout the last 35 years (see threats we have discussed. All but one similar human-caused threats occur to discussion under ‘‘Declines in the model evaluating changing climatic the subspecies’ habitat in areas in Northern Mexican Gartersnake Native patterns for the southwestern United proximity to human population centers Fish Prey Base’’ within Listing Factor States and northern Mexico predict a in Mexico, and (2) a time-lagged effect, C). The decline of native fish species drying trend for the region (Seagar et al. with respect to nonnative species that depend on native riparian and 2007, pp. 1181–1184). We acknowledge invasions, within more remote habitat aquatic systems provides evidence of that drought and the loss of surface in Mexico as postulated in Unmack and overall impacts to the affected biotic water in riparian and aquatic Fagan (2004, pp. 233–243). communities. These effects were communities are related to changing Based on museum records found in discussed in detail in Factor A and climatic conditions (Seagar et al. 2007, Holycross et al. (2006, Appendix F), we Factor C above. pp. 1181–1184). The extent to which expect the northern Mexican In response to the impacts to the changing climate patterns will affect the gartersnake retained its entire historic northern Mexican gartersnake and its northern Mexican gartersnake is not distribution within the United States native prey base discussed above and in known with certainty at this time. through the 1920s and likely into the our analysis of threats, the distribution However, threats to the northern 1930s. Activities such as the of northern Mexican gartersnake has Mexican gartersnake indentified in construction of dams and water been reduced to approximately 10 Factors A and C will likely be diversions that occurred throughout the percent of its historic range within the exacerbated by changes to climatic early to mid-1900s for agriculture and United States over the last 80 years. patterns in the southwestern United regional economic development likely However, because of the sensitivity of States due to resulting increasing eliminated surface flow throughout the northern Mexican gartersnake to drought and reduction of surface waters stream reaches with occupied habitat, community-wide effects from nonnative if the predicted patterns are realized. which led to subsequent and species, we believe the most significant Data specific to changes in climatic widespread extirpations of northern period of declines and subsequent patterns in Mexico are limited, but Mexican gartersnake populations in extirpations of entire populations likely because the models for the southwestern areas such as the lower Gila and Salt coincided with the proliferation of United States included northern rivers in Arizona. nonnative species beginning in the Mexico, we believe that the effect from After the period of dam construction 1940s and 1950s, most notably with the the changing climatic patterns will and the subsequent creation of widespread introduction and expansion exacerbate threats due to Factors A and reservoirs, widespread nonnative fish of sportfish such as largemouth bass, C in that country as well. stocking efforts ensued throughout green sunfish, and channel and flathead Arizona beginning during the mid catfish. In addition, further declines and Foreseeable Future 1900’s. In the Verde River system alone, extirpations likely resulted from When determining whether a species Rinne et al. (1998, p. 3) estimated that systematic bullfrog introductions, is in danger of extinction throughout all over 5,300 independent stocking actions beginning in the 1970s and early 1980s, or a significant portion of its range, or occurred that involved 12 different caused by the bullfrog’s natural capacity is likely to become in danger of species of nonnative fish species since to disperse and its predation behavior extinction in the foreseeable future, we the 1930s and 1940s. If we extrapolate on the northern Mexican gartersnake must identify that foreseeable future for that effort over the same timeframe for and associated prey base. In several the species. The Act does not other historically occupied, larger-order areas where northern Mexican specifically define the term ‘‘foreseeable systems known as recreational fisheries gartersnakes remain in the United future.’’ In discussing the concept of such as the Salt, upper Gila, Colorado, States, we have observed skewed age- foreseeable future for the northern Santa Cruz, Agua Fria, and San Pedro class distributions within populations Mexican gartersnake, we considered (1) rivers, Tonto and Oak creeks, and other that favor large-bodied, older the biological and demographic tributaries with significant flow individuals with significantly less characteristics of the species (such as throughout central and southern newborns and juveniles (Holm and generation times, population genetics, Arizona, in addition to the other private Lowe 1995, pp. 33–34; Holycross et al. trends in age-class distribution within stockings of stock tanks and other 2006, pp. 41–44; Wallace et al. 2008, pp. current populations, etc.); (2) our ability isolated habitat, the magnitude of the 243–244). These trends are particularly to predict or extrapolate the effects of nonnative species invasion over this apparent in areas where habitat remains threats facing the species into the future; timeframe becomes clear. Subsequent to structurally intact, but where nonnative and (3) the relative permanency or these efforts, but to a lesser extent, the species maintain stable populations. irreversibility of these threats. Of the spread of bullfrogs and crayfish, both The observed effects of nonnative threats to the northern Mexican purposefully and incidentally, species on age-class distribution and gartersnake and its prey base that have commenced during the 1970s and 1980s recruitment are an important influence been discussed above in our analysis of (Tellman 2002, p. 43). We estimate that on the maintenance of current the threats, we believe the threat of near 100 percent of the habitat that populations to be considered in our nonnative species presents the most historically supported northern Mexican evaluation of the foreseeable future for widespread, imminent, and serious gartersnakes has been invaded over- this species. We were not able to locate threat to the long-term sustainability of time, either purposefully or indirectly any quantitative studies on longevity of this subspecies. Therefore, we through dispersal, by nonnative species the northern Mexican gartersnake in the concentrate primarily upon this threat whether they be nonnative fish, wild, or on gartersnakes in general. to the northern Mexican gartersnake in bullfrogs, or crayfish. The effects from However, Bowler (1975) recorded our analysis of the subspecies’ viability this influx of nonnative species longevity of amphibians and reptiles in into the foreseeable future. Because our throughout the American Southwest captivity that included several species
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within the genus Thamnophis. gartersnakes from each litter may reach the northern Mexican gartersnake, in its Lifespans of six different gartersnake reproductive age. Whether or not these entirety, will be extirpated from the species ranged from 2 to 10 years individuals find a mate and successfully United States during this time frame (Bowler 1975). These data are old, reproduce depends upon the population because it would remain plausible that however, and innovations in the captive density and the degree of threats that extremely low-density populations of a care of specimens in the subsequent may be acting on a given population. few individuals may persist in other three decades have improved our In Table 4 of Holycross et al. (2006, areas past this time frame. knowledge of captive husbandry for p. 64), capture rates of northern Considering the above discussion on these species, allowing longer lifespans Mexican gartersnakes during surveys in (1) reproduction biology, observed in captivity. Simply knowing that 2004 and 2005 along the Mogollon Rim trends in population demographics, and individuals of a certain species are of Arizona were compared to those from age-class survivorship; (2) the time capable of living a certain number of a previous study, Rosen and Schwalbe periods that correlated to the onset of years under ideal captive conditions (1988, Appendix I). In total, capture the most significant threats to the means that longevity in the wild might rates in nine different stream reaches species and number of years it has taken be longer than suspected, although surveyed by both sets of investigators for a 90 percent reduction of the usually shorter than in captivity. Ernst were compared. Rosen and Schwalbe distribution of the subspecies in the and Zug (1996, p. 39) provide one (1988, Appendix I) spent 128 person- United States; (3) the relative isolation record on wild longevity in the common search hours to capture a total of 10 and disjunct nature of current gartersnake (Thamnophis sirtalis) as individuals at six of the nine (66 populations and their inability to serve nine years. It is reasonable to conclude percent) stream reaches. Holycross et al. as a basis for genetic exchange; (4) that the northern Mexican gartersnake, a (2006, p. 64) spent 142 person-search comparative analysis between similarly sized snake of the same genus, hours [11 percent more than Rosen and comprehensive survey results spread may have similar longevity in the wild. Schwalbe (1988, Appendix I)] and over 17 years over a significant portion found six total individuals in only two of the subspecies’ historical distribution The average age of sexual maturity is stream reaches of the nine (22 percent) in the United States and subsequent 2.5 years for female northern Mexican that were comparably surveyed. These extrapolations for remaining gartersnakes, and 2 years for males. data indicate that Holycross et al. (2006, populations; and (5) the future potential Females may only breed once every 2 p. 64) found northern Mexican for threats most detrimental to the long- years (Rosen and Schwalbe 1988, pp. gartersnakes at 66 percent fewer term viability of the subspecies in the 16–17). Considering these timeframes, a locations than did Rosen and Schwalbe United States (such as the continued female northern Mexican gartersnake (1988, Appendix I) which indicate proliferation of nonnative species), we might reproduce up to three times potential population extirpations in anticipate that northern Mexican during a maximum lifespan in the wild. two-thirds of populations during that gartersnake may be predominantly We are aware of no studies on the 17-year time period. The averaged extirpated from the U.S. within 25 survivorship of northern Mexican number of person-search hours per years. We base this estimate largely gartersnakes in the wild. However, capture was 12.8 hours in 1988 (Rosen upon our most current observations of Jayne and Bennett (1990, pp. 1209– and Schwalbe 1988, Appendix I), but population trends and their response to 1221) studied survivorship within a approximately twice that (23.6 person- threats posed by nonnative species, as population of common gartersnakes, a search hours) in 2004–2005 (Holycross discussed above. similar species, and found that, in two et al. 2006, p. 64). We do not expect that current policies groups of similarly aged snakes within Today, there remain three areas in the on native fish restoration and recovery that population, survivorship during the United States where the northern will change. These policies now focus first year following birth was 29 percent Mexican gartersnake is most reliably activities on replacing fisheries which and 43 percent in this 2-year study, found, the Upper Santa Cruz River in contain nonnative species with wholly although we are unaware of the the San Rafael Valley of south-central native fisheries in stream types that are presence, type, or extent of threats that Arizona, Tonto Creek from the vicinity generally not suitable for northern may have influenced survivorship. Only of Gisela downstream to Roosevelt Lake, Mexican gartersnakes, rather than 16 percent of one group survived into and the Page Springs/Bubbling Ponds mainstem rivers of lower gradient which their second year, while 50 percent of hatchery complex along Oak Creek provide preferred habitat for the the second group survived into their slightly upstream of its confluence with northern Mexican gartersnake. We have second year (Jayne and Bennett 1990, the Verde River. These populations are also discussed in Factor C above the pp. 1209–1221). Jayne and Bennett geographically disjunct, genetically widespread influence of crayfish and (1990, pp. 1209–1221) calculated that 15 isolated from one-another, and lack bullfrogs on riparian and aquatic percent of individuals live to be older significant, nearby source populations communities and the significant than 2 years. Adult survival rates in to serve as a natural source of difficulty of removing them from areas common gartersnakes appears to be individuals for recolonization should once they have become established. As quite variable, however. In Manitoba, any one of them become extirpated. discussed in Factor E, climate change adult year-to-year survivorship was Therefore, these populations remain and subsequent drought will likely calculated at 34 percent and at 67 highly vulnerable to the effects of the exacerbate the threats to the northern percent in the Northwest Territories threats discussed in detail in Factors A– Mexican gartersnake related to habitat (Larsen and Gregory 1989, pp. 84–85; E above, and to stochastic events not and prey base. Thus, the foreseeable Larsen et al. 1993, pp. 338–342). Based previously anticipated. If we extrapolate future for the northern Mexican on demographic studies on the common the last 20 years of population trends gartersnake in the U.S. is 25 years to gartersnake and making a conservative documented in the previous paragraph, 2033. estimate on survivorship and fecundity we anticipate that in approximately 15– With respect to the species’ rates without consideration of the 20 years, these remaining, currently foreseeable future throughout its presence or degree of threats, it is reliable populations may become distribution in Mexico, threats to the reasonable to presume that, on average, extirpated should current trends persist northern Mexican gartersnake from two individual northern Mexican into the future. This is not to say that human-related activities are most likely
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in areas adjacent to human population species because it contributes certain types of habitat that are centers, and these threats affect the meaningfully to the representation, necessary for the species to carry out its subspecies to a similar degree as resiliency, or redundancy of the species. life-history functions, such as breeding, observed in the United States. We The contribution must be at a level such feeding, migration, dispersal, or conclude that changes to climatic that its loss would result in a decrease wintering. patterns will affect northern Mexican in the ability of the species to persist. Redundancy of populations may be gartersnake habitat in similar ways in The first step in determining whether needed to provide a margin of safety for the more northern latitudes of Mexico as a species is threatened or endangered in the species to withstand catastrophic has been anticipated for the a significant portion of its range is to events. This concept does not mean that southwestern United States. Therefore, identify any portions of the range of the any portion that provides redundancy is we estimate the foreseeable future in species that warrant further per se a significant portion of the range populated areas of Mexico within the consideration. The range of a species of a species. The idea is to conserve range of the subspecies to be 25 years. can theoretically be divided into enough areas of the range so that Unmack and Fagan (2004, p. 233) portions in an infinite number of ways. random perturbations in the system hypothesized that a time-lagged effect is To identify portions that warrant further only act on a few populations. occurring in portions of Mexico with consideration, we determine whether Therefore, we examine each area based respect to nonnative species invasions, there is substantial information on whether that area provides an due primarily to the remoteness of some indicating that (1) the portions may be increment of redundancy that is areas. However, there is widespread significant, and (2) the species may be important to the conservation of the consensus that it is inevitable that in danger of extinction there or likely to species. nonnative species will continue to become so within the foreseeable future. Adequate representation ensures that invade new habitats throughout Mexico, In practice, a key part of this analysis is the species’ adaptive capabilities are leading to further declines and whether the threats are geographically conserved. Specifically, we evaluate a extirpations of the northern Mexican concentrated in some way. If the threats range portion to see how it contributes gartersnake and its prey species in to the species are essentially uniform to the genetic diversity of the species. Mexico (Conant 1974, pp. 471, 487–489; throughout its range, no portion is likely The loss of genetically based diversity Contreras Balderas and Lozano 1994, to warrant further consideration. may substantially reduce the ability of pp. 383–384; Miller et al. 2005, pp. 60– Moreover, if any concentration of the species to respond and adapt to 61; Abarca 2006; Luja and Rodrı´guez- threats applies only to portions of the future environmental changes. A Estrella 2008, pp. 17–22). Consequently, range that are unimportant to the peripheral population may contribute for the more remote areas of Mexico, the conservation of the species, such meaningfully to representation if there foreseeable future may be beyond 2033, portions will not warrant further is evidence that it provides genetic but we are not confident estimating how consideration. diversity due to its location on the far beyond. If we identify any portions that margin of the species’ habitat warrant further consideration, we then requirements. Significant Portion of the Range determine whether the species is Based upon factors that contribute to Analysis threatened or endangered in any our analysis of whether a species or As required by the Act, we considered significant portion. If we determine that subspecies is ‘‘In Danger of Extinction the five potential threat factors to assess a portion of the range is not significant, Throughout All or a Significant Portion whether the northern Mexican we do not determine whether the of Its Range,’’ and in consideration of gartersnake is threatened or endangered species is threatened or endangered the status of and threats to the northern throughout all or a significant portion of there. Mexican gartersnake discussed its range. When considering the listing The terms ‘‘resiliency,’’ previously, we find that significant status of the species, the first step in the ‘‘redundancy,’’ and ‘‘representation’’ are threats to the continued existence of the analysis is to determine whether the intended to be indicators of the northern Mexican gartersnake occur species is in danger of extinction conservation value of portions of the throughout all of its range in the United throughout all of its range. If this is the range. Resiliency of a species allows it States and Mexico. Therefore, it is not case, then we list the species in its to recover from periodic disturbances. A necessary to conduct further analysis entirety. For instance, if the threats to a species will likely be more resilient if with respect to the significance of any species are directly acting on only a large populations exist in high-quality portion of its range at this time. portion of its range, but they are at such habitat that is distributed throughout its a large scale that they place the entire range in a way that captures the Finding species in danger of extinction, we environmental variability available. A We have carefully examined the best would list the entire species. portion of the range of a species may scientific and commercial information We next consider whether any make a meaningful contribution to the available regarding the past, present, significant portion of the northern resiliency of the species if the area is and future threats faced by the northern Mexican gartersnake range meets the relatively large and contains particularly Mexican gartersnake. We reviewed the definition of endangered or is likely to high-quality habitat, or if its location or petition, information available in our become endangered in the foreseeable characteristics make it less susceptible files, other published and unpublished future (threatened). On March 16, 2007, to certain threats than other portions of information submitted to us during the a formal opinion was issued by the the range. When evaluating whether or public comment periods following our Solicitor of the Department of the how a portion of the range contributes 90-day and previous 12-month petition Interior, ‘‘The Meaning of ‘In Danger of to resiliency of the species, we evaluate findings and consulted with recognized Extinction Throughout All or a the historical value of the portion and northern Mexican gartersnake experts Significant Portion of Its Range’ ’’ how frequently the portion is used by and other Federal, State, Tribal, and (USDOI 2007, pp. 1–36). A portion of a the species, if possible. The range Mexican resource agencies. On the basis species’ range is significant if it is part portion may contribute to resiliency for of the best scientific and commercial of the current range of the species and other reasons; for instance, it may information available, we find that is important to the conservation of the contain an important concentration of listing of the northern Mexican
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gartersnake as threatened or endangered defenseless against the effect of many of the species that rely upon throughout its range in the United States nonnative species invasions. them. and Mexico, based on its rangewide The decline of the northern Mexican In making this finding, we status, is warranted, due to the present gartersnake has been exacerbated by acknowledge that the Mexican or threatened destruction, modification historical and ongoing threats to its Government has found the Mexican or curtailment of its habitat; predation; habitat in the United States. The threats gartersnake to be in danger of and the inadequacy of existing identified and discussed above in detail disappearance in the short-or medium- regulatory mechanisms. However, as under Factor A include: (1) The term future in their country from the explained in more detail below, an modification and loss of ecologically destruction and modification of its immediate proposal of a regulation valuable riparian and aquatic habitat or from the effects of shrinking implementing this action is precluded communities; (2) urban and rural population sizes, or both, and has, by higher priority listing actions, and development; (3) road construction, use, therefore, listed the species as progress is being made to add or remove and maintenance; (4) human population Threatened, under the listing authority qualified species from the Lists of growth; (5) groundwater pumping, of SEMARNAT (SEDESOL 2001). We Endangered and Threatened Wildlife surface water diversions, and flood; (6) have provided an assessment of the and Plants. improper livestock grazing; (7) status of the northern Mexican We recognize there have been catastrophic wildfire and wildfire in gartersnake and its habitat in Mexico, remarkable declines in the distribution non-fire adapted communities; and (8) but we also rely on the assessment of and abundance of the northern Mexican undocumented immigration and the species made by the Mexican gartersnake within its distribution in the international border enforcement and Government in listing the entity as United States, which are primarily management. In addition, disease and Threatened. The available literature attributed to individual and community parasitism, climate change, and drought supports the assessment of the species interactions with nonnative species that may pose threats to the northern made by the Mexican Government, occur in every single locality where Mexican gartersnake and its prey base. which indicates that nonnative species As a result of our assessment, we find northern Mexican gartersnakes have and habitat modification and loss are that certain land use activities, such as been documented. We identified the adversely affecting the status of road construction and use, improper ecological mechanisms for which northern Mexican gartersnakes in livestock grazing, undocumented nonnative interactions occur to include: Mexico. immigration and associated Additionally, land uses, such as (1) Direct predation on northern international border enforcement and urbanization and development, Mexican gartersnakes by nonnative management activities, and some types improper livestock grazing, water species; and (2) the effects of a of development, pose a more significant diversions and groundwater pumping, diminished prey base via nonnative risk to highly fragmented, low-density and impoundments, have resulted in species preying upon and competing populations of northern Mexican losses of vegetative cover, deforestation, with native prey species as documented gartersnakes, particularly in the erosion, and pollution that have in a large body of scientific research, presence of nonnative species. We know modified or destroyed historical which is cited and analyzed in our of no current population of northern northern Mexican gartersnake habitat in discussion of threats under each of the Mexican gartersnakes in the United Mexico. Collectively, the impacts of listing factors. States that does not occur in the traditional rural land management Throughout the range of the northern presence of nonnative species. practices and growth of the economic Mexican gartersnake, literature In this finding, we have emphasized sector, infrastructure, and population documents the cause and effect the importance of the protection of the growth are expected to continue into the relationship of modification of the food ecosystems upon which the northern future. chains within native riparian and Mexican gartersnake depends, and We have reviewed the available aquatic communities. The substantial documented the status of riparian and information to determine if the existing decline of primary native prey species, aquatic communities in the and foreseeable threats pose an such as leopard frogs and native fish, southwestern United States and much of emergency. We have determined that an has contributed significantly to the Mexico. Evidence of the current emergency listing is not warranted for decline of a primary predator, the precarious status of native riparian and this subspecies at this time because, northern Mexican gartersnake. In this aquatic ecosystems in the southwestern within the current distribution of the respect, the northern Mexican United States is the proportion of subspecies in Mexico, there are at least gartersnake is considered an indicator riparian or aquatic obligate species that some populations of the northern species, or a species that can be used to are either federally listed under the Act Mexican gartersnake that exist in gauge the condition of a particular or candidates for listing. In Arizona, relatively natural conditions that are habitat, community, or ecosystem. The there is a total of 73 species that meet unlikely to change in the short-term. synergistic effect of nonnative species these criteria. Of these 73 species, 38 (52 However, if at any time we determine both reducing the prey base of, and percent) are riparian or aquatic. Of the that emergency listing of the northern directly preying upon, northern 45 vertebrate species that are either Mexican gartersnake is warranted, we Mexican gartersnakes has placed federally listed or candidates for listing will initiate an emergency listing. significant pressure upon the viability in Arizona, 30 (67 percent) have The Service adopted guidelines on and sustainability of current northern riparian or aquatic life histories, and 19 September 21, 1983 (48 FR 43098) to Mexican gartersnake populations and (42 percent) are potential northern establish a rational system for allocating has led to significant fragmentation and Mexican gartersnake prey species in available appropriations to the highest risks to the continued viability of larval, juvenile, or adult forms, based on priority species when adding species to current populations. The evolutionary overlapping historical distributions. the Lists of Endangered or Threatened biology of the northern Mexican These data suggest that the riparian and Wildlife and Plants or reclassifying gartersnake, much like that of native aquatic ecosystems in Arizona, upon threatened species to endangered status. fish and leopard frogs, has left the which the northern Mexican gartersnake The system places greatest importance species without adaptation to and depends, cannot currently support on the immediacy and magnitude of
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threats, but also factors in the level of and publishing documents; and mandated critical habitat designations, taxonomic distinctiveness by assigning obtaining, reviewing, and evaluating Congress and the courts have in effect priority in descending order to public comments and peer review determined the amount of money monotypic genera, full species, and comments on proposed rules and available for other listing activities. subspecies (or equivalently, distinct incorporating relevant information into Therefore, the funds in the listing cap, population segments of vertebrates). As final rules. The number of listing other than those needed to address a result of our analysis of the best actions that we can undertake in a given court-mandated critical habitat for available scientific and commercial year also is influenced by the already listed species, set the limits on information, we have assigned the complexity of those listing actions; that our determinations of preclusion and northern Mexican gartersnake a Listing is, more complex actions generally are expeditious progress. Priority Number of 3, based on high more costly. For example, during the Congress also recognized that the magnitude and immediacy of threats. past several years, the cost (excluding availability of resources was the key One or more of the threats discussed publication costs) for preparing a 12- element in deciding whether, when above is occurring in each known month finding, without a proposed rule, making a 12-month petition finding, we population in the United States and has ranged from approximately $11,000 would prepare and issue a listing throughout historically occupied for one species with a restricted range proposal or instead make a ‘‘warranted habitats in Mexico. These threats are and involving a relatively but precluded’’ finding for a given ongoing and, in some cases (e.g., uncomplicated analysis to $305,000 for species. The Conference Report nonnative species), considered another species that is wide-ranging and accompanying Public Law 97–304, irreversible. While we conclude that involving a complex analysis. which established the current statutory listing the northern Mexican gartersnake We cannot spend more than is deadlines and the warranted-but- is warranted, an immediate proposal to appropriated for the Listing Program precluded finding, states (in a list this species is precluded by other without violating the Anti-Deficiency discussion on 90-day petition findings higher priority listing, which we Act (see 31 U.S.C. 1341(a)(1)(A)). In that by its own terms also covers 12- address below. addition, in FY 1998 and for each fiscal month findings) that the deadlines were year since then, Congress has placed a ‘‘not intended to allow the Secretary to Preclusion and Expeditious Progress statutory cap on funds which may be delay commencing the rulemaking Preclusion is a function of the listing expended for the Listing Program, equal process for any reason other than that priority of a species in relation to the to the amount expressly appropriated the existence of pending or imminent resources that are available and for that purpose in that fiscal year. This proposals to list species subject to a competing demands for those resources. cap was designed to prevent funds greater degree of threat would make Thus, in any given fiscal year (FY), appropriated for other functions under allocation of resources to such a petition multiple factors dictate whether it will the Act (for example, recovery funds for [that is, for a lower-ranking species] be possible to undertake work on a removing species from the Lists), or for unwise.’’ proposed listing regulation or whether other Service programs, from being used In FY 2008, expeditious progress is promulgation of such a proposal is for Listing Program actions (see House that amount of work that could be warranted but precluded by higher- Report 105–163, 105th Congress, 1st achieved with $8,206,940, which is the priority listing actions. Session, July 1, 1997). amount of money that Congress The resources available for listing Recognizing that designation of appropriated for the Listing Program actions are determined through the critical habitat for species already listed (that is, the portion of the Listing annual Congressional appropriations would consume most of the overall Program funding not related to critical process. The appropriation for the Listing Program appropriation, Congress habitat designations for species that are Listing Program is available to support also put a critical habitat subcap in already listed). Our process is to make work involving the following listing place in FY 2002 and has retained it our determinations of preclusion on a actions: proposed and final listing rules; each subsequent year to ensure that nationwide basis to ensure that the 90-day and 12-month findings on some funds are available for other work species most in need of listing will be petitions to add species to the Lists of in the Listing Program: ‘‘The critical addressed first and also because we Endangered and Threatened Wildlife habitat designation subcap will ensure allocate our listing budget on a and Plants (Lists) or to change the status that some funding is available to nationwide basis. The $8,206,940 was of a species from threatened to address other listing activities’’ (House used to fund work in the following endangered; annual determinations on Report No. 107–103, 107th Congress, 1st categories: Compliance with court prior ‘‘warranted but precluded’’ Session, June 19, 2001). In FY 2002 and orders and court-approved settlement petition findings as required under each year until FY 2006, the Service has agreements requiring that petition section 4(b)(3)(C)(i) of the Act; proposed had to use virtually the entire critical findings or listing determinations be and final rules designating critical habitat subcap to address court- completed by a specific date; section 4 habitat; and litigation-related, mandated designations of critical (of the Act) listing actions with absolute administrative, and program habitat, and consequently none of the statutory deadlines; essential litigation- management functions (including critical habitat subcap funds have been related, administrative, and listing preparing and allocating budgets, available for other listing activities. In program management functions; and responding to Congressional and public FY 2007, we were able to use some of high-priority listing actions. The inquiries, and conducting public the critical habitat subcap funds to fund allocations for each specific listing outreach regarding listing and critical proposed listing determinations for action are identified in the Service’s FY habitat). The work involved in high-priority candidate species; 2008 Allocation Table (part of our preparing various listing documents can however, in FY 2008 we were unable to administrative record). be extensive and may include, but is not do this due to our workload for For FY 2009, on September 23, 2008 limited to: Gathering and assessing the designating critical habitat. Congress passed a Continuing best scientific and commercial data Thus, through the listing cap, the Resolution to operate the Federal available and conducting analyses used critical habitat subcap, and the amount government at the FY 2008 level of as the basis for our decisions; writing of funds needed to address court- funding through March 6, 2009 (Pub. L.
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110–329). Although we are currently have had the highest priority to receive gartersnake is a subspecies, we assigned developing the allocations for specific funding to work on a proposed listing it an LPN of 3 (the highest category listing actions that we will fund during determination. As we work on proposed available for a subspecies). Therefore, FY 2009, we anticipate funding work to listing rules for these 40 candidates, we work on a proposed listing comply with court orders and court- are applying the ranking criteria to the determination for the northern Mexican approved settlement agreements, work next group of candidates with LPN of 2 gartersnake was, and will continue to be on statutorily required petition findings, and 3 to determine the next set of in the next year, precluded by work on final listing determinations for those highest priority candidate species. higher priority candidate species species that were proposed for listing To be more efficient in our listing (species with LPN of 2); listing actions with funds from FY 2008, and process, as we work on proposed rules with absolute statutory, court ordered, continued work on proposed listing for these species in the next several or court-approved deadlines; and final determinations for high-priority species. years, we are preparing multi-species listing determinations for those species proposals when appropriate, and these In FY 2007, we had more than 120 that were proposed for listing with may include species with lower priority funds from FY 2008. This work includes species with an LPN of 2, based on our if they overlap geographically or have September 21, 1983, guidance for all the actions listed in the tables below the same threats as a species with an under expeditious progress. assigning an LPN for each candidate LPN of 2. In addition, available staff species (48 FR 43098). Using this resources are also a factor in As explained above, a determination guidance, we assign each candidate an determining high-priority species that listing is warranted but precluded LPN of 1 to 12, depending on the provided with funding. Finally, must also demonstrate that expeditious magnitude of threats, imminence of proposed rules for reclassification of progress is being made to add or remove threats, and taxonomic status; the lower threatened species to endangered are qualified species to and from the Lists the LPN, the higher the listing priority lower priority, since as listed species, of Endangered and Threatened Wildlife (that is, a species with an LPN of 1 they are already afforded the protection and Plants. (We note that we do not would have the highest listing priority). of the Act and implementing discuss specific actions taken on Because of the large number of high- regulations. progress towards removing species from priority species, we further ranked the We assigned the northern Mexican the Lists because that work is conducted candidate species with an LPN of 2 by gartersnake an LPN of 3, based on our using appropriations for our Recovery using the following extinction-risk type finding that the subspecies faces program, a separately budgeted criteria: International Union for the immediate and high magnitude threats component of the Endangered Species Conservation of Nature and Natural from the present or threatened Program. As explained above in our Resources (IUCN) Red list status/rank, destruction, modification or curtailment description of the statutory cap on Heritage rank (provided by of its habitat; predation; and the Listing Program funds, the Recovery NatureServe), Heritage threat rank inadequacy of existing regulatory Program funds and actions supported by (provided by NatureServe), and species mechanisms. One or more of the threats them cannot be considered in currently with fewer than 50 discussed above are occurring in each determining expeditious progress made individuals, or 4 or fewer populations. known population in the United States in the Listing Program.) As with our Those species with the highest IUCN and throughout historically occupied ‘‘precluded’’ finding, expeditious rank (critically endangered), the highest habitats in Mexico. These threats are on- progress in adding qualified species to Heritage rank (G1), the highest Heritage going and, in some cases (e.g., nonnative the Lists is a function of the resources threat rank (substantial, imminent species), considered irreversible. available and the competing demands threats), and currently with fewer than Pursuant to the 1983 Guidelines, a for those funds. Our expeditious 50 individuals, or fewer than 4 ‘‘species’’ facing imminent high- progress in FY 2008 in the Listing populations, comprised a list of magnitude threats is assigned an LPN of Program included preparing and approximately 40 candidate species 1, 2, or 3 depending on its taxonomic publishing the following (‘‘Top 40’’). These 40 candidate species status. Because the northern Mexican determinations:
FY 2008 COMPLETED LISTING ACTIONS
Publication date Title Actions FR pages
10/09/2007 ...... 90-Day Finding on a Petition to List the Notice of 90-day Petition Finding, 72 FR 57278–57283. Black-Footed Albatross (Phoebastria Substantial. nigripes) as Threatened or Endangered. 10/09/2007 ...... 90-Day Finding on a Petition To List the Notice of 90-day Petition Finding, 72 FR 57273–57276. Giant Palouse Earthworm as Threatened Not substantial. or Endangered. 10/23/2007 ...... 90-Day Finding on a Petition To List the Notice of 90-day Petition Finding, 72 FR 59983–59989. Mountain Whitefish (Prosopium Not substantial. williamsoni) in the Big Lost River, ID, as Threatened or Endangered. 10/23/2007 ...... 90-Day Finding on a Petition To List the Notice of 90-day Petition Finding, 72 FR 59979–59983. Summer-Run Kokanee Population in Not substantial. Issaquah Creek, WA, as Threatened or Endangered. 11/08/2007 ...... Response to Court on Significant Portion of Response to Court ...... 72 FR 63123–63140. the Range, and Evaluation of Distinct Population Segments, for the Queen Charlotte Goshawk.
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FY 2008 COMPLETED LISTING ACTIONS—Continued
Publication date Title Actions FR pages
12/13/2007 ...... 12-Month Finding on a Petition To List the Notice of 12-month Petition Find- 72 FR 71039–71054. Jollyville Plateau salamander (Eurycea ing, Warranted but Precluded. tonkawae) as Endangered With Critical Habitat. 1/08/2008 ...... 90-Day Finding on a Petition To List the Notice of 90-day Petition Finding, 73 FR 1312–1313. Pygmy Rabbit (Brachylagus idahoensis) Substantial. as Threatened or Endangered. 1/10/2008 ...... 90-Day Finding on Petition To List the Notice of 90-day Petition Finding, 73 FR 1855–1861. Amargosa River Population of the Mojave Substantial. Fringe-Toed Lizard (Uma scoparia) as Threatened or Endangered With Critical Habitat. 1/24/2008 ...... 12-Month Finding on a Petition To List the Notice of 12-month Petition Find- 73 FR 4379–4418. Siskiyou Mountains Salamander ing, Not Warranted. (Plethodon stormi) and Scott Bar Sala- mander (Plethodon asupak) as Threat- ened or Endangered. 2/05/2008 ...... 12-Month Finding on a Petition To List the Notice of 12-month Petition Find- 73 FR 6660 6684. Gunnison’s Prairie Dog as Threatened or ing, Warranted. Endangered. 02/07/2008 ...... 12-Month Finding on a Petition To List the Notice of Review ...... 73 FR 7236 7237. Bonneville Cutthroat Trout (Oncorhynchus clarki utah) as Threat- ened or Endangered. 02/19/2008 ...... Listing Phyllostegia hispida (No Common Proposed Listing, Endangered ...... 73 FR 9078 9085. Name) as Endangered Throughout Its Range. 02/26/2008 ...... Initiation of Status Review for the Greater Notice of Status Review ...... 73 FR 10218 10219. Sage-Grouse (Centrocercus urophasianus) as Threatened or Endan- gered. 03/11/2008 ...... 12-Month Finding on a Petition To List the Notice 12 month petition finding, 73 FR 12929 12941. North American Wolverine as Endan- Not warranted. gered or Threatened. 03/20/2008 ...... 90-Day Finding on a Petition To List the Notice of 90-day Petition Finding, 73 FR 14950 14955. U.S. Population of Coaster Brook Trout Substantial. (Salvelinus fontinalis) as Endangered. 04/29/2008 ...... 90-Day Finding on a Petition to List the Notice of 90-day Petition Finding, 73 FR 23170 23172. Western Sage-Grouse (Centrocercus Substantial. urophasianus phaios) as Threatened or Endangered. 04/29/2008 ...... 90-Day Finding on Petitions To List the Notice of 90-day Petition Finding, 73 FR 23173 23175. Mono Basin Area Population of the Substantial. Greater Sage-Grouse (Centrocercus urophasianus) as Threatened or Endan- gered. 05/06/2008 ...... Petition To List the San Francisco Bay- Notice of 90-day Petition Finding, 73 FR 24611 24915. Delta Population of the Longfin Smelt Substantial. (Spirinchus thaleichthys) as Endangered. 05/06/2008 ...... 90-Day Finding on a Petition to List Notice of 90-day Petition Finding, 73 FR 24915 24922. Kokanee (Oncorhynchus nerka) in Lake Substantial. Sammamish, Washington, as Threatened or Endangered. 05/06/2008 ...... 12-Month Finding on a Petition to List the Notice of Status Review ...... 73 FR 24910 24911. White-tailed Prairie Dog (Cynomys leucurus) as Threatened or Endangered. 05/15/2008 ...... 90-Day Finding on a Petition To List the Notice of 90-day Petition Finding, 73 FR 28080 28084. Ashy Storm-Petrel (Oceanodroma Substantial. homochroa) as Threatened or Endan- gered. 05/15/2008 ...... Determination of Threatened Status for the Final Listing, Threatened ...... 73 FR 28211 28303. Polar Bear (Ursus maritimus) Throughout Its Range; Final Rule. 05/15/2008 ...... Special Rule for the Polar Bear; Interim Interim Final Special Rule ...... 73 FR 28305 28318. Final Rule. 05/28/2008 ...... Initiation of Status Review for the Northern Notice of Status Review ...... 73 FR 30596 30598. Mexican Gartersnake (Thamnophis eques megalops). 06/18/2008 ...... 90-Day Finding on a Petition To List the Notice of 90-day Petition Finding, 73 FR 34686 34692. Long-Tailed Duck (Clangula hyemalis) as Not substantial. Endangered.
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FY 2008 COMPLETED LISTING ACTIONS—Continued
Publication date Title Actions FR pages
07/10/2008 ...... 90-Day Finding on a Petition To Reclassify Notice of 90-day Petition Finding, 73 FR 39639 39643. the Delta Smelt (Hypomesus Substantial. transpacificus) From Threatened to En- dangered. 07/29/2008 ...... 90-Day Finding on a Petition To List the Notice of 90-day Petition Finding, 73 FR 43905 43910. Tucson Shovel-Nosed Snake (Chionactis Substantial. occipitalis klauberi) as Threatened or En- dangered with Critical Habitat. 8/13/2008 ...... Proposed Endangered Status for Reticu- Proposed Critical Habitat, Pro- 73 FR 47257 47324. lated Flatwoods Salamander; Proposed posed Listing, Endangered. Designation of Critical Habitat for Frosted Flatwoods Salamander and Reticulated Flatwoods Salamander. 9/9/2008 ...... 12-month Finding on a Petition to List the Notice 12 month petition finding, 73 FR 52235 52256. Bonneville Cutthroat Trout as Threatened Not warranted. or Endangered. 10/15/2008 ...... 90-Day Finding on a Petition To List the Notice of 90-day Petition Finding, 73 FR 61007 61015. Least Chub. Substantial. 10/21/2008 ...... Listing 48 Species on Kauai as Endangered Proposed Listing, Endangered; 73 FR 62591 62742. and Designating Critical Habitat. Proposed Critical Habitat. 10/24/2008 ...... 90-Day Finding on a Petition to List the Notice of 90-day Petition Finding, 73 FR 63421 63424. Sacramento Valley Tiger Beetle as En- Not substantial. dangered. 10/28/2008 ...... 90-Day Finding on a Petition To List the Notice of 90-day Petition Finding, 73 FR 63919 63926. Dusky Tree Vole (Arborimus longicaudus Substantial. silvicola) as Threatened or Endangered.
Our expeditious progress also timelines, that is, timelines required they overlap geographically or have the included work on listing actions, which under the Act. Actions in the bottom same threats as the species with the were funded in FY 2008, but have not section of the table are high priority high priority. Including these species yet been completed. These actions are listing actions. These actions include together in the same proposed rule listed below. We have completed all work primarily on species with an LPN results in considerable savings in time work funded in FY 2008 on all actions of 2, and selection of these species is and funding as compared to preparing under a deadline set by a court. Actions partially based on available staff separate proposed rules for each of them in the middle section of the table are resources, and when appropriate, in the future. being conducted to meet statutory include species with a lower priority if
ACTIONS FUNDED IN FY 2008 BUT NOT COMPLETED
Species Action
Actions Subject to Court Order/Settlement Agreement
NONE ...... NONE.
Actions with Statutory Deadlines
Phyllostegia hispida ...... Final listing. Yellow-billed loon ...... 12-month petition finding. Black-footed albatross ...... 12-month petition finding. Mount Charleston blue butterfly ...... 12-month petition finding. Goose Creek milk-vetch ...... 12-month petition finding. Mojave fringe-toed lizard ...... 12-month petition finding. White-tailed prairie dog ...... 12-month petition finding. Pygmy rabbit (rangewide) ...... 12-month petition finding. Black-tailed prairie dog ...... 90-day petition finding. Lynx (include New Mexico in listing) ...... 90-day petition finding. Wyoming pocket gopher ...... 90-day petition finding. Llanero coqui ...... 90-day petition finding. American pika ...... 90-day petition finding. Sacramento Mts. checkerspot butterfly ...... 90-day petition finding. 206 species ...... 90-day petition finding. 475 Southwestern species ...... 90-day petition finding.
High Priority Listing Actions
21 Oahu candidate species (16 plants, 5 damselflies) (18 with LPN =2, 3 with LPN = Proposed listing. 3, 1 with LPN =9).
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ACTIONS FUNDED IN FY 2008 BUT NOT COMPLETED—Continued
Species Action
3 southeast aquatic species (Georgia pigtoe, interrupted rocksnail, rough hornsnail) 1 Proposed listing. (all with LPN = 2). Casey’s june beetle (LPN = 2) ...... Proposed listing. Sand dune lizard (LPN = 2) ...... Proposed listing. 2 southwest springsnails (Pyrgulopsis bernadina (LPN = 2), Pyrgulopsis trivialis (LPN Proposed listing. = 2)). 3 southwest springsnails (Pyrgulopsis chupaderae (LPN = 2), Pyrgulopsis gilae (LPN Proposed listing. = 11), Pyrgulopsis thermalis (LPN 11)). 2 mussels (rayed bean (LPN = 2), snuffbox No LPN) ...... Proposed listing. 2 mussels (sheepnose (LPN = 2), spectaclecase (LPN = 4),) ...... Proposed listing. Ozark hellbender 2 (LPN = 3) ...... Proposed listing. Altamaha spinymussel (LPN = 2) ...... Proposed listing. 4 southeast fish (rush darter (LPN = 2), chucky madtom (LPN = 2), Cumberland dart- Proposed listing. er (LPN = 5), laurel dace (LPN = 5)). 2 Colorado plants (Parchute beardtongue (Penstemon debilis) (LPN = 2), Debeque Proposed listing. phacelia (Phacelia submutica) (LPN = 8)). Pagosa skyrocket (Ipomopsis polyantha) (LPN = 2) ...... Proposed listing. 1 Funds for listing actions for 3 of these species were also provided in FY 2007. 2 We funded a proposed rule for this subspecies with an LPN of 3 ahead of other species with LPN of 2, because the threats to the species were so imminent and of a high magnitude that we considered emergency listing if we were unable to fund work on a proposed listing rule in FY 2008.
We have endeavored to make our review will determine if a change in Author listing actions as efficient and timely as status is warranted, including the need possible, given the requirements of the to make prompt use of emergency listing The primary author of this notice is relevant law and regulations, and procedures. the Arizona Ecological Services Office constraints relating to workload and We intend that any proposed listing (see FOR FURTHER INFORMATION CONTACT personnel. We are continually action for the northern Mexican section). gartersnake will be as accurate as considering ways to streamline Authority processes or achieve economies of scale, possible. Therefore, we will continue to such as by batching related actions accept additional information and The authority for this action is section together. Given our limited budget for comments from all concerned 4 of the Endangered Species Act of implementing section 4 of the Act, these governmental agencies, the scientific 1973, as amended (16 U.S.C. 1531 et actions described above collectively community, industry, or any other seq.). interested party concerning this finding. constitute expeditious progress. Dated: November 12, 2008. References Cited The northern Mexican gartersnake Kenneth Stansell, will be added to the list of candidate A complete list of all references cited Acting Director, U.S. Fish and Wildlife species upon publication of this 12- in this document is available upon Service. month finding. We will continue to request from the Field Supervisor at the [FR Doc. E8–27524 Filed 11–24–08; 8:45 am] monitor the status of this species as new Arizona Ecological Services Office (see information becomes available. This ADDRESSES section). BILLING CODE 4310–55–P
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