Conservation Status and Sex Ratios of the Coahuila Box Turtle (Terrapene coahuila) in the Cuatro Ciénegas Valley of Coahuila, Mexico, 2011–2018

The Coahuila box turtle (Terrapene coahuila Schmidt and Owens 1944) is a largely aquatic member of the North American box turtle genus Terrapene. The species is listed as Endangered by the International Union for Conservation of Nature (IUCN) Red List (van Dijk et al. 2007), as Endangered by the US Endangered Species Act (US Fish and Wildlife Service 1973), and as a Species of Special Protection by the Mexican government (Secretária del Medio Ambiente y Recursos Naturales 2001). It is also listed among the 50 most threatened tortoise and freshwater turtle species by the IUCN Species Survival Commission Tortoise and Freshwater Turtle Specialist Group (Turtle Conservation Coalition [TCC] 2018). Terrapene coahuila has one of the most restricted distributions of any turtle in the Western Hemisphere. It is endemic to spring-fed arid-land pools and shallow wetlands in the intermontane valley of Cuatro Ciénegas and the Cuatro Ciénegas Wildlife Protected Area (CCPA) in Coahuila, northern Mexico. The CCPA is an 84,000-ha protected zone that is surrounded by the 1.5 million-ha Área de Protección de Recursos Naturales. The Cuatro Ciénegas valley is a highly endangered arid-land spring ecosystem that features at least 9 endemic fish species, as well as 3 endemic turtles (Brown, 1968, 1971, 1974; Howeth and Brown 2011). Although there is still some debate about the taxonomic relationships within the genus Terrapene (Stephens and Wiens 2003), genetic and morphological data indicate that T. coahuila is most closely related to Terrapene carolina (Milstead 1960; Minx 1996; Feldman and Parham 2002; Stephens and Wiens 2008).

Terrapene coahuila occurs in dozens of permanent and seasonal wetlands and hundreds of small pools in the Chihuahuan desert ecosystem of the Cuatro Ciénegas valley (Howeth and Brown 2011). It occurs mainly in and around wetlands, but may migrate hundreds of meters or even kilometers across land (Howeth et al. 2008). The habitat in the CCPA is severely threatened by water table alteration; the land surrounding the reserve has been given over to large-scale crop production. In addition to habitat loss, poaching exists; illegally collected T. coahuila are reported each year and unknown numbers are kept as pets in the town of Cuatro Ciénegas. Current population estimates do not exist for T. coahuila. Brown (1974) estimated a total species population of approximately 10,000 individuals and a population density of 148 turtles/ha, extrapolated from a mark–recapture study in a single wetland in the valley. Nearly 40 yrs later, Howeth and Brown (2011) estimated a far lower density of 0.60–0.67 turtles/ha based on capture effort. These densities yielded an estimate of 2500 turtles remaining (van Dijk et al. 2007), a 75% decline in the population over a 40-yr period. Brown (1974) found that half of his study population of marked turtles were recaptured in a wetland other than the one in which they had been marked in the same wetland complex. Howeth's study (2008) indicated only 10% of individuals had moved within a wetland complex and < 1% had moved between wetlands. These long-distance migrations have important implications for the gene flow and conservation genetics of this species (see McGaugh 2012).

Water diversion using canals and pumping has lowered the water table in the area, and the shallow nature of the springs and their distance from water sources in local mountains has already resulted in significant wetland habitat loss (Howeth and Brown 2011). Ongoing agricultural and urban development in the area is being carried out without consideration for the effects that efficient water diversion will have on the remaining habitat (Castañeda Gaytán et al. 2015).

In this study our goal was to estimate population densities of the species and record any changes since the last survey was done (see Howeth and Brown 2011), in order to make an estimate of the total population remaining. In addition, we recorded sex ratios in the remaining wetlands to evaluate the population's demographic structure, as recent brief surveys indicated a strong preponderance of males in the remaining populations (Castañeda Gaytán et al. 2014, 2015).

METHODS

Estimating the population size of T. coahuila was challenging because the turtle is semiaquatic and its habitat and behavior change from wet season to dry season. In the dry season, turtles can be found in ponds in both shallow and deeper water and hidden under sedges and grasses in open moist fields (Howeth and Brown 2011). In the wet season, turtles occur in ponds but can also be found in semiflooded grassy areas across the Cuatro Ciénegas valley (Fig. 1). We walked transects through each wetland site and also collected mark–recapture data. There were already an estimated 350 T. coahuila bearing individual filed notches from previous field studies. We surveyed wetlands within 8 sampling sites, as previously established in Salas-Westphal et al. (2011): Los Gatos, Charcos Prietos I, Charcos Prietos 2, Poza Orozco, Pozas Azules, Poza La Tecla, Angostura, and Churince.

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Transect surveys were carried out twice a month for each wetland site from July 2011 to November 2015 and then at irregular intervals through September 2018. Monitoring of the Pozas Azules transect was conducted only during the month of July due to changes in the entry policies of researchers by the nonprofit organization Pronatura Northeast A.C. As a result of these changes, some continuity in the established transect was lost.

Transects were established taking into consideration the extent and geometry of the habitat in order to maintain a constant search effort within preferred habitat types. Five 100-m-long transects followed the contours of the wetland but always included vegetation types preferred by T. coahuila (Salas-Westphal et al. 2011; Castañeda Gaytán et al. 2014, 2015), including those in standing water. The transect was walked by teams of 5–7 researchers at distances of 3–5 m apart twice a day, yielding a final transect of 1 km. Transects were walked from 0700 to 1300 hrs. If the abundance of turtles was high, search time was extended. Morphometric measures of individuals were taken following the protocol of Salas-Westphal et al. (2011). Males exhibited brown eye color with a deep central concavity in the plastron, while females were yellow-eyed without a plastron depression. To examine a potential sex ratio bias in the population, we employed a binomial test based on total captures (Wilson and Hardy 2002).

Estimation of potential range-wide distribution via environmental niche modeling was done using a MAX ENT algorithm with 11 bioclimatic layers (Biolayers 2, 3, 4, 6, 7, 8, 9, 12, 14 and 15) and taking into account terrain elevation. Bioclimatic layers were assigned according to Cuervo-Robayo et al. (2013) using meteorological data from 1910 to 2009 and were considered more appropriate for Mexican ecozones than standard WorldClim layer categories. A wetland layer was not considered because that habitat type is highly dynamic and varies widely among seasons and years. Autocorrelated layers (Pearson correlation coefficient > 0.75) were deleted from the analysis to avoid bias. Most of the data (n = 215 locations; 75%) were used for constructing the model and the remaining 72 locations (25%) was used to validate it. Five hundred iterations were carried out and 10 final replicates with the highest AUC (area under the curve) values were analyzed to evaluate biological congruency with the species and the habitat. A total of 287 records of T. coahuila found in the study site were included in the potential distribution analysis, and we assumed geographic separation among data points to avoid redundancy. Pixel size was 100 × 100 m in order to include topographic variations in elevation and water level.

RESULTS

We encountered 393 T. coahuila encountered during surveys from 2011 to 2018, 51 (13%) of which were animals previously marked in the present study. The Los Gatos wetland had the highest population density of T. coahuila; Churince and Angostura had the lowest; and Orozco, Pozas Azules, and Churinces had declining densities over the study period (Tables 1 and 2). We recorded 162 different animals at Los Gatos, of which 47 were females, 111 were males, and 4 were unsexed. Abundance of turtles in the wetlands corresponded with recorded densities (Fig. 2). Terrapene coahuila densities were greater in the wetlands farthest from human activity. Los Gatos had the highest abundance of T. coahuila and Churince and Angostura had the lowest. One site of low density, Churince, has since 2011 dried up due to a lowering of the water table caused in all likelihood by irrigation for agriculture outside the protected area. As of 2018, Churince is a dry site with the carcasses of all 3 endemic freshwater turtle species but no live turtles present.

Table 1 Densities of Terrapene coahuila (individuals per hectare) recorded in 8 wetlands in the Cuatro Ciénegas valley from 2011 to 2015. nd = not determined.

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Table 2 Regression test statistics for density estimation (2011–2015) for each location surveyed: p (= alpha error), df (= degree of freedom), slope equation, and r² value. No location showed a significant positive correlation between density and time.

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We estimated the area of suitable habitat for T. coahuila within the census area to be 539.76 ha. This estimate was based on our model indicating that approximately 0.6% of the CCPA is habitat suitable for T. coahuila (Fig. 3). Elevation (31.2%), isotherm (26.6%), and precipitation (18.5%) layers explained current potential distribution for the species within the CCPA. This habitat represents 0.003% of the land area of the state of Coahuila and 0.6% of the land area of the CCPA.

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The average population density based on the transects over the entire study period was 3.3 turtles/ha, yielding an estimate of a total of 1791 T. coahuila in the census area. The population showed a significant departure from 1:1 sex ratio (0.61, 95% CI: 0.56–0.66, binomial test, n = 382 individual turtles; p < 0.025; Fig. 4). Of all turtles captured and marked, males represented 61% (n = 235) of the sample and females represented 38% (n = 147). Juvenile T. coahuila were seen only twice during the entire survey. Eleven additional animals (2.8%) were not sexed due to ambiguous sexual characteristics.

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DISCUSSION

Although different sampling methods make a direct comparison to Brown's (1974) census data difficult, the population of T. coahuila in the Cuatro Ciénegas valley has declined over the past several decades. Los Gatos wetland had the highest density of turtles during this and previous studies and must be considered the most important site for the continued survival of T. coahuila. From the time of Howeth's (2008) study, a decade passed until our own survey and census work. Our overall population estimate is lower than hers and 80% lower than Brown's (1974) estimate from the 1970s.

Greater habitat modification in the form of wetland reduction and livestock grazing was associated with fewer turtles. There have been further reductions in the water table since the 1970s, leading to habitat loss that continues to negatively impact T. coahuila populations and threaten their continued survival. Howeth and Brown (2011) documented several wetlands from the 1970s that had dried up and were no longer T. coahuila habitat in the early 2000s. This habitat modification has continued, with the effect that more of Brown's study areas are today dry and lacking in turtles altogether. The drying of seasonally marshy areas noted by Hendrickson et al. (2008) and Howeth and Brown (2011) now extends to the Churince system wetlands, in which we found no living turtles but the carcasses and skeletal remains of many during 2018. This area west of Sierra de San Marcos supported a genetically distinct subpopulation of T. coahuila (Howeth et al. 2008) and its loss of wetland habitat therefore jeopardizes the future genetic viability of the species.

Diversion of water from the valley for human use has been occurring for decades. The nominal federal protection from the Mexican government has not prevented the installation of irrigation canals, pipelines, and other forms of water diversion crossing the valley, which have contributed greatly to draining the aquifer and damaging the biodiversity of at least 9 endemic fish species native to the area (Hendrickson et al. 2008). Large-scale agricultural projects outside the protected area drain the water table under the protected area; unless water rights are obtained, none of the wetland areas are safe from drainage, even if legally protected or converted formally to sanctuary status.

The male-biased sex ratio was unexpected and of conservation concern. Brown (1974) had documented a 1:1 sex ratio. Immature individuals are normally secretive and difficult to find, but discovering only 2 juveniles during more than 6 yrs of surveying suggests that recruitment is low. We have anecdotal evidence of increased presence of predators such as coyote, foxes, and raccoons, perhaps subsidized by human population growth in the valley. A systematic investigation of the population status and diets of these and other predatory species is warranted.

Continued drops in the water table within the CCPA severely threaten the continued existence of the species. Human population growth in the town of Cuatro Ciénegas has long threatened the valley ecosystem. Invasive plants (especially Arundo donax and Phragmites australis) are also a problem in T. coahuila habitat, where they choke shallow shoreline areas that are the preferred habitat of the turtles. Direct collection of the turtles by people occurs and the intensive poaching of other species of Terrapene across Mexico for export to the Asian pet market remains a concern.

Moreover, tourism has increased markedly in recent years and land developers are buying land within the CCPA with hopes of developing it. There are currently plans to build a golf course and a water park adjacent to the protected area, with concerns from the government and conservationists that the water needs of these and other tourism developments will ultimately lower the water table further and destroy much of the habitat remaining for T. coahuila and other aquatic and semiaquatic biota.

We recommend the following steps for the long-term preservation of T. coahuila habitat in the Cuatro Ciénegas Valley:

• 1)

  Stronger protection of the wetland habitats remaining across the Cuatro Ciénegas Valley.

• 2)

  Upgrading the threat status of Terrapene coahuila from Endangered (van Dijk et al. 2007, Criteria A, B, C, and D) to Critically Endangered. Our data suggest a small number of adults, a reduction of the population since the last study, and little recruitment of juveniles (Criteria A, B, and C). These data, combined with an overall population increasingly fragmented by urban and agricultural development, justify elevating the threat status of the species.

• 3)

  Our ongoing research has identified the areas of highest T. coahuila density in the Cuatro Ciénegas valley. Efforts must be made to secure long-term protection for this land from development. Other wetlands with lower densities but great conservation potential should be strategically acquired to maintain dispersal corridors and maximize genetic diversity. Experimental habitat restoration is also being planned, through acquiring water rights under wetland habitat and pumping water via windmills.

• 4)

  Because of the small size of the captive population of this species (54 individuals in the North American Association of Zoos Aquariums studbook as of 2019; Barnhart and Putnam 2017) and the lack of any captive breeding programs in Mexico, we advocate establishing multiple captive assurance colonies and are in the process of doing so. Progeny from these projects may potentially be reintroduced to wetlands that have been depopulated. Breeding stock can also be obtained as donated pets, so initiating a public awareness campaign that encourages local people to donate current pets to assurance colonies could be successful.

• 5)

  Continued field studies on behavior and reproductive biology are essential to understand the causes of the skewed sex ratio observed in this species and possible consequences to future population size.

Tribute to Peter C.H. Pritchard

We are honored to have this article included in an issue dedicated to the memory of the late Peter Pritchard. All of us in the chelonian research world owe a debt of gratitude to Pritchard for his lifetime of work promoting the study and conservation of turtles and tortoises. The senior author (Stanford) knew Peter, and his books and words inspired him to follow his passion to make the study and conservation of these wonderful animals a reality.