The Conservation Status of Several Endemic Mexican Kinosternid Turtles
Abstract
The goal of this project was to carry out surveys in northern and central México to locate extant populations of Kinosternon hirtipes chapalaense, K. h. magdalense, and K. h. megacephalum, evaluate their conservation status, help establish captive breeding colonies of these taxa in the near future, and collect tissues for phylogenetic studies. During 2010 and 2011, we were able to locate extant populations of 2 of the subspecies (K. h. chapalaense and K. h. magdalense), but K. h. megacephalum could not be found. We also failed to locate natural springs in a radius of approximately 60 km from the type locality (and only known locality) of K. h. megacephalum and believe that this turtle is extinct.
Kinosternon hirtipes is a small, extremely aquatic turtle that inhabits permanent water bodies in southern Texas and northern México, and on the Mexican plateau. Six subspecies are currently recognized (hirtipes, murrayi, chapalaense, magdalense, megacephalum, and tarascense), 4 of them occur in small, isolated drainages in north-central México and the southern margin of the Mexican plateau (Iverson 1981). Much of the habitat of K. hirtipes has been greatly altered in the past 200 yrs, mainly as a result of water diversion for agriculture, expansion of population centers, desiccation of aquifers, pollution, and the introduction of alien species (Rosen 2008). Three of the known subspecies are of special concern, because they have not been reported in scientific collections for many years and their habitats have been especially altered in recent years (Rosen 2008). Kinosternon hirtipes chapalaense is known from Lake Chapala and Laguna Zapotlán in the states of Jalisco and Michoacán. Kinosternon hirtipes magdalense inhabits Presa San Juanico in northwestern Michoacán. Kinosternon hirtipes megacephalum is only known from 8 specimens collected during 1961 by Bryce C. Brown and John Wottring in springs south of Viesca, southern Coahuila. This subspecies is believed to be extinct due to desiccation of its habitat during the 1960s, whereas the 2 other subspecies have not been found in the past 30 yrs (Iverson 1981). During 2010 and 2011, we spent approximately a month doing fieldwork in northern and central México. Our goal was to locate extant populations of these 3 subspecies and evaluate their conservation status.
METHODS
Trapping and Seining
Turtle traps were hand-made by using chicken wire, according to the protocol proposed by Iverson (1979). Traps were baited with canned tuna fish, fresh fish, or pig liver. Traps were submerged halfway and left overnight or were completely submerged and checked every 1 or 2 hrs. We used 2 commercial seining nets (1.5 × 4.5 m) for seining. Seining was carried out by 2 people in shallow areas of rivers and lakes.
Measurements, Tissues, and Markings
Turtles were measured to the nearest 0.1 mm with the use of a vernier caliper. The following measurements were taken: midline carapace length, carapace width at widest point, maximum plastron length, and plastron width at the bridge (posterior width of the forelobe). Turtles were also weighed to the nearest gram. Sex was determined in adult turtles by the presence of elevated scales on the back of the thigh in male K. hirtipes. We used a modified version of Cagle's technique (1939) for marking turtles by making incisions in the marginal scutes of the shell. A sample of tissue was taken from the turtles by cutting a small piece of skin from the interdigital membrane of the hind foot for future DNA analysis. The tissues were stored in 96% ethanol or in lysis buffer. Two samples were taken from each turtle. Turtles caught were transported to temporary facilities in Colima, México.
Area of Study
We focused our search efforts in 4 different areas, located in central and northern México. Each is described below.
Lago de Chapala (states of Jalisco and Michoacán) is the largest freshwater lake in México, 80 km in length, with an area of approximately 1146 km2 (Comisión Estatal del Agua de Jalisco 2012). It is relatively shallow (no deeper than 10 m) and connects 2 of the largest rivers in México, the Rio Lerma and Rio Santiago. The Rio Lerma flows into the eastern end of Lake Chapala, whereas Rio Santiago exits the lake from the northeastern end of the lake. Both K. h. chapalaense and Kinosternon integrum are known from Lake Chapala, but K. h. chapalaense has not been collected in the lake since 1978 (Iverson 1981). We visited the lake on 20 occasions between 2010 and 2011, mostly during the summer, but additional trips were made in December and January 2011 and 2012. We deployed more than 20 turtle traps at 11 different localities (Fig. 1).
Citation: Chelonian Conservation and Biology 12, 1; 10.2744/CCB-1017.1
Laguna de Zapotlán (state of Jalisco) is a small lake located north of Ciudad Guzman in southern Jalisco. Nine specimens of K. h. chapalaense have been collected from the lake but none in recent years. We visited the Laguna de Zapotlán during July of 2010. Several traps were placed at 3 localities across the lake, at irrigation canals south of the lake, and at a small stream that flowed into the lake at its north end, for a total of 5 trapping localities.
Presa San Juanico (state of Michoacán) is located at the northwestern end of the state of Michoacán, in the municipality of Cotija de la Paz. Only 7 specimens of K. h. magdalense have been collected (3 live specimens, 4 shells), all of them along the dam at the eastern end of the presa. According to Iverson (1981), when he visited the lake in 1978 and again in 1981, the water level was very low, and no turtles were found in his 1981 trip, so he questioned the survival of this subspecies. We spent a week at San Juanico during the summer of 2010.
The Viesca basin and surrounding areas (states of Coahuila, Zacatecas, and Durango) are one of the driest areas in México, with less than 200 mm of rain a year (Garcia 1998). It is located in northern México, in the state of Coahuila, south of the town of Viesca. This area used to have a series of springs, which, according to local residents, supported an abundant diversity of life, much like the Cuatro Cienegas springs in northern Coahuila; however, the springs at Viesca dried during the 1960s as a result of indiscriminate water extraction to irrigate agricultural fields in the adjacent Laguna area of Torreón, Coahuila. Only 8 specimens of K. h. megacephalum were collected at the springs before they dried up (Iverson 1981). Since then, no additional specimens have been found. With the use of satellite images from Google Earth (Google Inc, 2009), we located several areas where natural springs could possibly be found. We spent a week at and near Viesca during the summer of 2010. Our main goal was to locate permanent bodies of water in the surrounding mountains in an effort to find extant populations of this turtle. We set traps and seined 10 different localities in the vicinity of Viesca.
RESULTS
Lago de Chapala
Most of our trapping and seining efforts were spent along the northwest end of the lake, between the towns of Chapala and Jocotepec. We also seined and trapped at a small pond, probably spring fed, northeast of San Antonio Tlayacapan. A map with the study areas is shown in Fig. 1. No turtles were found in more than 500 trapping plus seining hours. We visited the local fish market at Chapala, but no turtles were found for sale because river turtles are not usually consumed in this part of México. We talked with several fishermen at the lake, and they informed us that they do see turtles but infrequently. Four K. integrum were found crossing the roads along the north end of the lake, but none were caught in traps or by seining.
Laguna de Zapotlán
In a total of 96 trapping hours, only a male and a female K. h. chapalaense were caught, both from a stream at the north end of the lake (Fig. 2). This is the first time that the subspecies has been found since the late 1970s. A single K. integrum was also trapped at the same locality, which is the first time that the species has been reported from the lake. We also set traps at a small stream at Laguna Sayula, to the north of Laguna Zapotlán, and near Tapalpa, in the mountains to the west of the laguna, but no turtles were secured. Measurements of the K. h. chapalaense and K. integrum found at Zapotlán are given in Table 1.
Citation: Chelonian Conservation and Biology 12, 1; 10.2744/CCB-1017.1
Presa San Juanico
We set turtle traps at 17 localities in or near Presa San Juanico, including at the Rio Cotija and at 2 irrigation canals east of the presa. More than 360 hrs of trapping and seining produced a total of 5 K. h. magdalense, 2 juveniles and 3 adults (see Fig. 2). Four additional turtles were caught in fishermen's nets, 3 K. h. magdalense and 1 K. integrum. Kinosternon hirtipes magdalense had not been found since 1978 and its survival was uncertain. This is the first time that K. integrum has been caught at Presa San Juanico. Measurements of the K. h. magdalense and K. integrum found at San Juanico are given in Table 1.
Viesca
We explored the mountains south, east, and west of Viesca, as well as the area around Parras (to the east of Viesca), where natural springs once existed. We first explored the area south of Viesca, as Iverson proposed in 1981, to look for permanent water bodies. We followed a dry riverbed that is located in the mountains just south of Viesca. According to local residents, 2 man-made ponds existed in this area at one time, and it was possible to fish at this spot. When we visited the area, the ponds were gone, and no permanent water was to be found. We then headed southeast to the small towns of La Fe, Bajio de Ahuichila, San Juan de los Charcos, Nuevo Tampico, and La Presa, but no permanent water was found, only man-made ponds, where we seined and set turtle traps. The local residents knew of no permanent water in the area. We then visited the small town of La Peña, located to the northeast of Viesca. A small pond at this locality had been visited in the past by both ichthyologists and herpetologists, and produced no turtles (Iverson 1981). We trapped and seined this place for several days, but only a single Kinosternon durangoense was trapped. We were told that the pond is periodically dried out for cleaning and that a single turtle of great proportions (perhaps Trachemys sp.) used to live there but was taken to the town of Parras a few years ago. The pond at La Peña is fed from a very small stream that comes out of a cave. Next, we headed to the town of La Rosita, in the mountains west of Viesca, because we were informed of a spring that came out of the Sierra Jimulco. We found several man-made ponds in the area, where we set traps and seined, but no turtles were found. When we reached the spring at Sierra Jimulco, we were disappointed to see that the water was being piped, and the spring was too small to support any turtles. Finally, we visited Parras and the mountains to the south. At Parras, the original springs have been turned into giant swimming pools that are frequently dried out for cleaning. We could find no turtles there. A worker at the pools told us that, at Arroyo de Moron, just south of Parras, in a place called “cañon de la Lima,” there are several tinajas that hold water year round. We explored the dry river bed for several kilometers but were unable to locate any water.
DISCUSSION
Kinosternon hirtipes chapalaense
Even though only 3 specimens were found at Laguna Zapotlán, this result is very encouraging, because the subspecies had not been found in more than 30 yrs. The Laguna Zapotlán is considered a Ramsar site, it is a refuge for approximately 25,000 waterfowl, and constitutes an important water reservoir in the region (Ramsar 2012). Even though the Laguna Zapotlán is considered biologically important for the region, it has been severely affected by human activities. Partially treated urban waste water from Ciudad Guzman and other towns is discharged into the lake, which contributes to its eutrophication (Ortiz-Jimenez et al. 2005; Greenberg 2009). Agricultural and urban runoff is also a major problem as well as sediment deposition caused by indiscriminate logging in the surrounding areas (Ortiz-Jimenez et al. 2005; Shear and de Anda 2009). As a result of the lake's eutrophication and sedimentation, plant species such as the cattail (Typha latifolia) and the invasive water hyacinth (Eichhornia crassipes) have become extremely abundant in the lake, and, at times, they have covered approximately 70% of the lake surface (Ortiz-Jimenez et al. 2005). Blooms of cyanobacteria and extremely high levels of Escherichia coli and other bacteria have been reported in recent years (Ortiz-Jimenez et al. 2005; Greenberg 2009). The long-term effects of human activities on the survival of K. h. chapalaense at Laguna Zapotlán cannot be established at present without further research. Water treatment at Ciudad Guzman will be essential to reduce the eutrophication of Laguna Zapotlán. Equally important will be the implementation of reforestation programs in the surrounding mountains to decrease sedimentation rates. Increasing water quality of the lake with these and other activities will be fundamental for the preservation of this important wetland, for improving the quality of life of local inhabitants, and for the survival of K. h. chapalaense and other aquatic fauna.
Chapala is the largest freshwater lake in México; it is a biologically rich area that supports a great number of species, including many endemic vertebrates. It is also a very important site for migratory species of birds (Ramsar 2012). The lake is fed by the Lerma River, which heads near the city of Almoloya del Rio in the state of México. From there, the river runs for approximately 965 km through the states of México, Michoacán, Querétaro, Guanajuato, and Jalisco. The water from the river has been diverted for agriculture, industries, and human consumption; some of the areas adjacent to the river are among México's most important agricultural as well as industrial centers, but most of the cities and industries in the area lack adequate water treatment plants. Due to a lack of treatment and indiscriminate water extraction, the Lerma River is now one of the most polluted rivers in the country (von Bertrab 2003). All this pollution ends up at Lake Chapala, where contamination levels have been extremely high (von Bertrab 2003). The city of Guadalajara, with more than 4 million inhabitants, obtains most of its water from Lake Chapala. Because of the excessive extraction of water from the Lerma Basin and the lake, the water level at Chapala has been greatly reduced on several occasions in the past 60 yrs, with extremely low levels recorded in 1954, 1991, and again from 2001 to 2004 (Comisión Estatal del Agua de Jalisco 2012). Erosion in the Lerma basin is also considered a major threat for the lake, which greatly affects the quality of water (von Bertrab 2003). Another important problem in the lake is the introduction of water hyacinth (E. crassipes), which has affected the original biota as well as economic activities in the lake (von Bertrab 2003). All these impacts on the lake's ecology might have a negative effect on the population of K. h. chapalaense, as has been the case in other North American turtle species that inhabit contaminated lakes (Bishop et al. 1991, 1998). Even though no turtles were trapped from the lake after intensive search efforts, we believe that the subspecies might still survive at Chapala, and perhaps trapping at other localities or a change in the trapping methods will eventually prove this. Ten species of fish are endemic to Chapala and the Lerma basin, including a freshwater lamprey (Lampetra spaficea) and 7 species of silversides (Chirostoma spp.) as well as the Popoche chub (Algansea popoche) and the Chapala chub (Yuriria chapalae) (Miller et al. 2003). Several of the species are now highly endangered because of the issues previously discussed (Jelks et al. 2008). The survival of these species as well as of K. h. chapalaense at Chapala will depend on adequate management of the lake, which that should focus on a more sustainable use of the water from both the lake and the Lerma basin as well as urgent actions to reduce the pollution and erosion, and to increase the removal of invasive vegetation.
Kinosternon hirtipes magdalense
It has now been shown that this subspecies is still extant at Presa San Juanico, where it had not been found since 1978 (Iverson 1981). The fact that this subspecies still survives in nature is encouraging, but several factors put this population at risk. When we visited the presa in the summer of 2011, the water level was extremely high, even corn fields adjacent to the lake had been inundated. The fisherman at San Juanico told us that the level of the presa had been very low during the past dry season, at about half the level of when we visited the lake. Those periods of very low water level could have a big impact on the population of K. h. magdalense. The possible eventual desiccation of the Presa San Juanico is by far the biggest threat to the survival of these turtles.
One of the most important economic activities at San Juanico is fishing. When we visited the area, there were 52 active fishermen at San Juanico. Most fishermen use gill nets, and they are known to cause turtle fatalities, because the turtles frequently get entangled in the nets and drown, as many fishermen reported to us. Another possible impact on the subspecies is the introduction of predatory fish into the lake. According to the fishermen, “bagre” (channel catfish, Ictalurus punctatus) were introduced around the year 2002, and they have observed them preying on hatchling turtles. Other species of introduced fish include tilapia (Oreochromis niloticus) and carp (Cyprinus carpio). The silverside fish Chirostoma melanoccus and Chirostoma reseratum are endemic to Presa San Juanico and are commercially harvested. Kinosternon integrum was not recorded from the Presa San Juanico in the late 1970s but is now there. The impact of this species on K. h. magdalense is not known. Fishermen at the presa are aware of the 2 different turtles, and they call them by different names, K. integrum is simply called “tortuga,” whereas K. h. magdalense is referred to as “chiquitortuga,” which means small turtle. We believe that this subspecies might also occur at a few other lakes and presas along the Magdalena Valley in Michoacán, but further fieldwork is needed to probe this. More specifically, collecting efforts should focus on the Laguna El Quiringual, northwest of Presa San Juanico, as well as at Presa Valle de Juarez, in neighboring Jalisco.
Kinosternon hirtipes megacephalum
Because the springs at Viesca dried during the 1960s, it was inferred that the turtle became extinct at that time, but no efforts had been made toward locating other permanent springs in the surrounding areas. Our expedition revealed that no permanent springs remain around Viesca and that the subspecies is almost certainly extinct. The excessive draining of water from aquifers in desert areas is a very common procedure that has a tremendous impact on nearby springs. Physical alteration of the habitat has been reported as the main cause of extinction of freshwater fishes in North America during the past century, and approximately 30 species have become extinct in the past 100 yrs (Miller et al. 1989). More and more water is being drained from aquifers in northern México to supply agricultural activities in the area, and this indiscriminate use of the water will have detrimental effects on other natural springs, such as the Cuatro Cienegas basin in northern Coahuila (Contreras-Balderas 1984; Anonymous 1998). Immediate measures should be put into action by the Mexican authorities to assure that other desert oases do not have the same fate as the Viesca springs and that other species do not follow K. h. megacephalum on the path of extinction.
Map showing the areas visited during this study.
(A) View of the stream flowing into Laguna Zapotlán; Kinosternon hirtipes chapalaense and Kinosternon integrum were trapped at this site. (B) Female K. h. chapalaense. (C) View of the mountains south of Viesca, no permanent water was found at this site. (D) Seining at an artificial pond southwest of Viesca. (E) View of laguna San Juanico from the eastern end. (F) Kinosternon hirtipes magdalense caught in a turtle trap at San Juanico.
