Reptiles of Banco Chinchorro: updated list, life history data, and conservation.
Biodiversity decline is a priority to both biology and the economy; some groups of organisms are used as bioindicators to determine the effects of climate change and habitat loss on species survival and also to model the future consequences on the ecological dynamic (Gibbons et al., 2000). Some of the bio-indicators selected are ectothermic organisms (reptiles, amphibians, fish, and insects) because their dependence on climatic factors, such as temperature and humidity, make them adequate models (Gibbons et al., 2000; Bickford et al., 2010). A recent study by Sinervo et al. (2010) predicts a massive decline of reptiles due to climate change over the next 65 years. Based on the thermal requirements of reptiles, it was determined that the most affected lizard species would be those inhabiting the warmest areas of the tropics (Huey et al., 2009; Sinervo et al., 2010). This hypothesis was based on the local extinction of Mexican lizards in the Yucatan Peninsula and promotes the study of their physiological requirements (i.e., temperature), to determine their vulnerability to climate change (Sinervo et al., 2010). However, basic information (ecological and physiological) on species inhabiting the Yucatan Peninsula is scarce (Charruau et al., 2015).
Nevertheless, Mexico has the most significant herpetofaunal diversity and endemism in Mesoamerica with 864 species of reptiles, representing 75% of Mesoamerican reptiles (1,148 species [Wilson and Johnson, 2010; Wilson et al., 2013; Flores-Villela and Garcia-Vazquez, 2014]). However, according to Wilson et al. (2013), this diversity is affected by deforestation (260,000 ha/year), which is one of the most determining factors in the decline of reptile biodiversity and justifies the importance of NPAs in biodiversity conservation. In Mexico, there are 176 NPAs covering >25,000,000 ha or 12% nationwide; whereas, 16 federal and 8 state reserves are located on the Caribbean coast of Quintana Roo, of which only 2 are categorized as Biosphere Reserve (Comision Nacional de Areas Naturales Protegidas http://www.conanp.gob.mx/). Conversely, island populations should be given special consideration for protection because most have little to no genetic flow with continental populations (Murphy and Mendez-de la Cruz, 2010). Additionally, island populations suffer different ecological and evolutionary pressures that promotes morphological, physiological, and behavioral differences from continental populations (Losos et al., 1997; Diaz de la Vega-Perez et al., 2013; Siliceo-Cantero and Garcia, 2014).
The Banco Chinchorro Biosphere Reserve (Banco Chinchorro BR), is an atoll located in the Caribbean region of Mexico 31 km from the southern coast of Quintana Roo (Fig. 1). The atoll has an important economic value for commerce and tourism; for example, Banco Chinchorro BR has been an important source of spiny lobster (Panulirus argus), queen conch (Strombus gigas) and commercially valuable fish species for >50 years (Miller, 1982; Aguilar-Perera and Aguilar-Davila, 1993; Instituto Nacional de Ecologia [INE], 2000; Hernandez et al., 2008). Tourism has increased in recent years, particularly for diving to see the impressively well-preserved reef structures and numerous culturally relevant ancient and modern shipwrecks found within the reserve (INE, 2000; Ardisson et al., 2011). Furthermore, isolation, traditional fishing methods, and the biosphere reserve status of the atoll have permitted the conservation of its ecosystems (Ardisson et al., 2011). Consequently, the atoll is an important site for the conservation of marine and terrestrial threatened habitats and animal species (INE, 2000; Ardisson et al., 2011).
Banco Chinchorro was declared a biosphere reserve by a decree published on 19 July 1996 (Secretaria de Medio Ambiente y Recursos Naturales [SEMARNAT] in Diario Oficial de la Federacion, 1996); a management plan for the reserve was published in 2000 (INE, 2000). This plan included a list of 14 reptile species that potentially inhabited the reserve (INE, 2000). However, some recent field observations in the cays of Banco Chinchorro cast doubt on the accuracy of this list.
[FIGURE 1 OMITTED]
Additionally, the category "biosphere reserve" is the highest level of priority to preserve as an NPA; is determined by the biological, ecological, and economic importance of a particular area; and can cover terrestrial and marine ecosystems. Those biosphere reserves are designated for research, education, economic improvement, and divulgation of information among the world web of NPA (United Nations Educational Scientific and Cultural Organization, http://www.unesco.org/). Therefore, the list of flora and fauna present is a priority to accomplish the functions of an NPA. Particularly, the Banco Chinchorro BR does not have a recent list of reptiles. Few studies have been done on reptiles of this reserve, with most studies mainly focused on crocodiles and parthenogenetic lizards (Manriquez-Moran et al., 2000; Charruau et al., 2005; Machkour-M'rabet et al., 2009; Charruau et al., 2010a, 2010b; Charruau, 2011, 2012; Perez-Flores et al., 2011; Charruau and Henaut, 2012; Charruau et al., 2012, 2013; Diaz de la Vega-Perez et al., 2013). On the other hand, it is important to mention that the State of Quintana Roo represents the highest developing rate in population growth and tourism development in Mexico. Therefore, the protected areas in this state should have proper management programs with accurate biodiversity information.
All previously mentioned arguments justify the protection of the Banco Chinchorro BR to protect the reptiles that inhabit this area. Therefore, the management plan of the reserve must be improved with accurate information about the reptiles present. We consider it relevant to investigate the reptiles of the atoll using techniques such as literature review, queries to scientific collections, interviews, and systematic field studies. Our objective was to reevaluate the reptile species present in the Banco Chinchorro BR and disseminate new life-history information for future research, in an effort to direct the conservation efforts and improve the current knowledge of reptiles of this important biological area.
MATERIALS AND METHODS--Banco Chinchorro Biosphere Reserve covers 144,360 ha including extensive coral reefs, reef lagoons, and adjacent oceanic waters. The atoll is separated from the continent by a canal of almost 1,000 m depth (United Nations Environment Programme/International Union for Conservation of Nature [UNEP/IUCN], 1988) and represents an important part of the Mesoamerican barrier-reef system with economic, educational, cultural, and biological-scientific relevance (INE, 2000; Ardisson et al., 2011). The reserve contains four cays: Cayo Lobos, Cayo Centro, and two cays of Cayo Norte with a total area of 582 ha, of which 435 ha are terrestrial habitats and 147 ha are interior lagoons. Cayo Norte is located at the extreme north of the reserve and consists of two cays (Cayo Norte Mayor and Cayo Norte Menor; Fig. 1) with a total area of 40 ha. Cayo Centro is the largest cay (541 ha) and is located in the center of the atoll 47 km from the mainland (Fig. 1). The fourth cay, located in the extreme south, is the 0.4 ha Cayo Lobos (Fig. 1). Cayo Centro and Cayo Norte are covered with different compositions of mangrove and halophytic or coastal dune vegetation (Fig. 1; Table 1). Cayo Lobos has coastal dune vegetation with Tournefortia gnaphalodes, Ipomoea alba, and Ipomoea pes-caprae (Table 1). The climate of Banco Chinchorro is warm subhumid with rains during summer and winter (Charruau, 2010).
Sampling Methods--We compiled a list of the reptile species present in Banco Chinchorro through literature review and direct observations during field work from 2011 to 2013 (throughout the four seasons). Additionally, PC and ADVP have worked on reptile ecology in Banco Chinchorro BR for 11 and 3 years, respectively. We conducted diurnal and nocturnal transect surveys of lizards and nocturnal surveys of crocodiles. We placed transects randomly along the islands, including paths connecting fishermen camps and each type of vegetation. On Cayo Centro, the main path extended from the southern tip of the island to [+ or -] 3.5 km to the north tip following the east coast of the island, corresponding to the most elevated part of the island (5 m). For Cayo Norte Menor and Mayor, the path surrounded each island. To complete the survey, we made random transects for each type of vegetation on each island. In Cayo Centro, we spent >250 days throughout the four seasons and estimate that we visited approximately 60% of the island. In Cayo Norte Mayor, we spent approximately 10 days working, visited almost 70% of the island, and went at Cayo Norte Menor two times (one day for each time) surveying almost 80% of the island. We did not visit Cayo Lobos. During these surveys, we captured crocodiles, iguanas, and small lizards using the noose technique (Fitzgerald, 2012). We identified all species using the most recent identification keys of Kohler (2008).
Morphological Data--For crocodiles, we sexed each individual captured using the observation of genital structures (presence or absence of penis) in the cloaca, and, for adult lizards, used observation of external sex-specific characteristics. We temporarily and individually marked lizards with a permanent marker on the abdomen and took them to the field station for measurements (total length [TL], snout-vent length [SVL], cranial length [CL], and mass [M]). We measured lengths in mm with an electronic stainless steel Vernier caliper ([+ or -] 0.1 mm; Truper S.A. de C.V., Ciudad de Mexico, D.F., Mexico) or with a tape measure ([+ or -] 1 mm) and mass in g with a micro-line spring scale ([+ or -] 0.1 g and [+ or -] 1 g; Pesola AG, Baar, Suisse). We released all organisms the following day at the site of capture, which we had previously georeferenced with a global positioning system (Garmin International Inc., Olathe, Kansas). The temporary mark permitted us to differentiate captures and recaptures.
Bibliographic, Scientific Collection, and Interviews Data--We searched the available literature on reptiles of Banco Chinchorro. Additionally, we searched and examined reptile specimens from Banco Chinchorro in museum collections from El Colegio de la Frontera Sur (ECOSUR), Instituto de Biologia of the Universidad Nacional Autonoma de Mexico, and Facultad de Ciencias of the Universidad Nacional Autonoma de Mexico. We collected voucher specimens of each species captured in Banco Chinchorro and deposited them in the reptile collection of ECOSUR campus Chetumal (ECO-CH-H). We also interviewed some fishermen and park rangers about the species they observed in Banco Chinchorro BR and about specific species such as boas, sea turtles, and house geckos. The interviews were made in a conversation form because fishermen are more "open" to that interview method, and we found that we obtain more information than with a standardized questionnaire. We were ensured that fishermen had accurately identified the species by showing them pictures or by questioning them about diagnostic characteristics of the species. We also talked with R. Herrera-Pavon, who previously studied sea turtles in the reserve, for additional information about turtle species.
Furthermore, we searched for the current protection and conservation status of each species listed by the IUCN (http:// www.iucn.org/), the Convention on International Trade in Endangered Species of Wild Fauna and Flora (2012; Appendices I, II, and III), and Mexican law (Secretaria de Medio Ambiente y Recursos Naturales [SEMARNAT], NOM-059-SEMARNAT-2010 in Diario Oficial de la Federacion, 2010).
RESULTS--Species Richness--We generated a list of 13 reptile species at Banco Chinchorro BR based on field work, literature, museum specimens, and interviews. These species are distributed in 12 genera, 8 families, and 4 orders (Table 2). The list consisted of one crocodilian, four marine turtles, two iguanas, two geckos, two anoles, one whiptail lizard, and one snake.
First, we updated and corrected the names of species appearing in the Banco Chinchorro BR Management Plan (BCMP). Hemidactylus tursicus was misspelled: the correct name is Hemidactylus turcicus. We also corrected an error in the spelling of the genus name for species Cnemitodhorus cozumela; the correct name of the genus is Cnemidophorus. However, at present, this genus is confined to the southern species, according to the phylogenetic hypothesis of Reeder et al. (2002); therefore, all northern species currently belong to the genus Aspidoscelis. In fact, the presence of Aspidoscelis cozumela is also a mistake because the species that occurs in Banco Chinchorro is Aspidoscelis maslini (we discuss more in the Discussion section).
We detected nine species of reptiles on our transects: Crocodylus acutus, Eretmochelys imbricata, Aristelliger georgeensis, Hemidactylus frenatus, Ctenosaura similis, Iguana iguana, Anolis allisoni, Anolis sagrei, and Aspidoscelis maslini. We observed Eretmochelys imbricata in the
reef lagoon 100 m from the west coast of Cayo Centro in a sea grass area. We observed Crocodylus acutus, Aristelliger georgeensis, Ctenosaura similis, Iguana iguana, Anolis allisoni, Anolis sagrei, and Aspidoscelis maslini in Cayo Norte and Cayo Centro. Hemidactylus frenatus is an abundant species and has only been detected at Cayo Centro on the walls of the field station. Similarly, an individual of Boa constrictor was recently captured (March 2015) in Cayo Centro (near of the lighthouse) by a team of the Grupo de Ecologia y Conservacion de Islas A.C. currently working in Cayo Centro to eliminate black rats (Rattus rattus). We never captured or observed Hemidactylus turcicus, Crocodylus moreletii, or other Anolis species that were mentioned in the previously compiled list. Voucher specimens of Aristelliger georgeensis, Anolis allisoni, A. sagrei, H. frenatus, and Aspidoscelis maslini have been deposited in the collection of ECOSUR museum (Table 3). The boa was taken to the Centro para la Conservacion e Investigacion de la Vida Silvestre of Bacalar (Quintana Roo), which is a part of the Secretaria del Medio Ambiente y Recursos Naturales (SEMARNAT).
From the museum collections, we found five species of reptiles collected in Banco Chinchorro identified as Crocodylus acutus (one skull), Anolis lemurinus (two specimens), A. allisoni (nine specimens), Aristelliger georgeensis (one specimen), and Hemidactylus turcicus (one specimen). These were deposited in the collections of ECOSUR or in the Facultad de Ciencias of the Universidad Nacional Autonoma de Mexico and have been collected in the reserve between 1996 and 2010 (Table 3). After review of the specimens, we detected some errors in identification. First, the reptile collection of ECOSUR museum included a specimen of Hemidactylus turcicus recently collected in Banco Chinchorro (in 2010). However, after a careful review of the specimen, it was identified as Hemidactylus frenatus. In addition, the two specimens of Anolis lemurinus deposited in the same collection were neonates of A. sagrei.
Based on the interviews with different staff from the reserve, we were able to identify nine species: Caretta caretta, Chelonia mydas, Eretmochelys imbricata, Crocodylus acutus, Aristelliger georgeensis, Ctenosaura similis, Iguana iguana, Anolis allisoni, and Aspidoscelis maslini (Table 2). None of the fishermen or park rangers interviewed had observed boas in Banco Chinchorro BR before March 2015. Furthermore, R. Herrera-Pavon told us that in addition to the presence of Caretta caretta, Chelonia mydas, and Eretmochelys imbricata, [greater than or equal to] 1 individual of Dermochelys coriacea had been captured, and other individuals observed, in the past in the Banco Chinchorro BR. Information obtained from the literature on reptiles of Banco Chinchorro BR is included in the discussion.
Ecological and Biological Data--We obtained morphological data for six species: Aristelliger georgeensis, Ctenosaura similis, Iguana iguana, Anolis allisoni, Anolis sagrei, and Aspidoscelis maslini (Table 4).
We captured specimens (11 males, 2 females, 4 young, and 3 hatchlings) of Aristelliger georgeensis at Cayo Centro and Cayo Norte Mayor at night between 2100h and 0120h. We captured them on the field station walls, on leaves of chit (Thrinax radiata) and coconut palms (Cocos nucifera), on branches of button mangrove (Conocarpus erectus), and in leaf litter. During the night, the color pattern of the specimens is grey or cream; and during the day, they adopt a chocolate brown color with white cream spots and lines.
We captured 78 Anolis allisoni (55 males and 23 females)--62 at Cayo Centro and 16 at Cayo Norte Mayor. Males and females are green, but are able to rapidly change to a dark brown color. Their eyes are capable of focusing on distinct objects. Males have dark lines on the body and limbs and can present a blue coloration from the head to the shoulders and anterior limbs during the green color phase, which is supposedly during the reproduction season. Males have a pink dewlap, while females do not. We captured or observed individuals on the walls of the field station and fishermen's houses; on leaves; and on trunks of vegetation, particularly chit and coconut palms, button mangrove, gumbo-limbo (Bursera simaruba), and blackbead (Pithecellobium keyense).
We captured 65 Anolis sagrei (54 males and 11 females)--40 from Cayo Centro and 25 from Cayo Norte Mayor. Males change their color from light grey to brown and black with white spots, and their dewlap colors are from yellow-orange with a red edge to orange-red. They can also present a crest along the top of the body. Similar to A. allisoni, their eyes are capable of focusing on distinct objects. Females present the same color variation but can also present a light vertebral stripe pattern of chevrons, bars, and spots. Females can also present a reduced dewlap. We captured or observed individuals on chit and coconut palms, gumbo-limbo, blackbead, dead dry trunk, leaf litter, and sand. In a recent study, individuals of A. sagrei have been found to present abscesses on their mouth, supposedly due to alimentation on ants and eggs of ants (Diaz de la Vega-Perez et al., 2014).
Aspidoscelis maslini was present at Cayo Norte and Cayo Centro, where we captured 6 and 40 individuals, respectively. We observed individuals on leaf litter and sand and found them actively foraging on insects during the hottest part of the day. They present light brown color at the dorsum and four yellow stripes each side of the dorsum; also present are long, white ventral scales. In some cases they also present a light blue color on the legs and tail. We observed females in gestation from March to May and, by palpation, could determine the presence of one to four eggs.
Ctenosaura similis were very abundant at Cayo Centro and Cayo Norte, especially around the field station and fishermen's camps. At Cayo Centro, fishermen and reserve staff feed them, which explains their abundance. In August 2011, we captured five males and one female at Cayo Centro. Males had a mean TL of 783.6 mm (651-954 mm) and a mean SVL of 328.8 mm (265-360 mm). Mean mass of two males weighed was 1,800 g. The female had an SVL of 250 mm and a mass of 500 g.
Iguana iguana was very abundant in Cayo Centro and Cayo Norte, and we observed individuals in great numbers around human construction where fishermen and reserve staff feed them. They were mainly observed on the ground, but often climbed to the top of coconut palms and ciricote (Cordia sebestena). In Cayo Centro, we captured six males and nine females in August 2011 and April 2012, respectively. Males had a mean TL of 1,470 mm (980-1,770 mm), a mean SVL of 484.2 mm (400-540 mm), and a mean mass of 5,940 g (3,000-8,500 g). Females had a mean TL of 1,089.3 mm (960-1,295 mm), a mean SVL of 357.2 mm (310-420 mm), and a mean mass of 1,866.3 g (1,000-3,500 g).
Based on our combined survey results and information gathered since 2003 by ADVP, we found that the overall sex ratio of the captured and sexed crocodiles with a TL >30 cm was 30 females for 99 males or 1:3.3. We observed some crocodiles in both cays of Cayo Norte (two in each cay), but no survey has been made at this time to determine the density of individuals. Soldiers of the Mexican navy based at Cayo Norte Mayor also reportedly observed crocodiles in this cay (Park rangers, pers. comm.). We also observed nests of Crocodylus acutus and Caretta caretta in Cayo Centro. We found 94 nests of Crocodylus acutus from 2006 to 2013. We found two nests of Caretta caretta in a fishermen camp in August 2007, and found one in May 2013.
Most of the species identified are oviparous, and only the Boa constrictor is viviparous. However, the composition of reptile species in this community is diverse in terms of sex determination of the embryos displaying genetic determination, temperature-dependent determination, facultative parthenogenesis, or obligated parthenogenesis (Table 2).
Protection and Conservation Status--Of the 13 reptile species identified at Banco Chinchorro BR, 9 (69%) are included on the IUCN Red List of threatened species with 7 presented at threatened status, 7 (54%) are in Convention on International Trade in Endangered Species of Wild Fauna and Flora Appendices, and 9 (69%) are protected by Mexican law (Secretaria de Medio Ambiente y Recursos Naturales [SEMARNAT], NOM-059SEMARNAT-2010 in Diario Oficial de la Federacion, 2010; Table 2). The two most endangered species are American crocodiles and sea turtles, which are classified as Vulnerable (Crocodylus acutus), Endangered (Caretta caretta, Chelonia mydas), or Critically Endangered (Eretmochelys imbricata and Dermochelys coriacea) by the IUCN (2015). We found two invasive species of lizards with no protection status (Hemidactylus frenatus and Anolis sagrei) and potentially one single Boa constrictor, which is categorized as threatened by Mexican protection law. Before this study, two geographically restricted lizards had no protection status by Mexican law (Anolis allisoni and Aspidoscelis maslini [Diaz de la Vega-Perez and Charruau, 2013; Diaz de la Vega-Perez and Mendez-de la Cruz, 2013]).
DISCUSSION--Diversity of Species--Our results, with 13 identified species of reptiles in the Banco Chinchorro BR, differ from the original list of 14 species of the BCMP. We did not observe the following species reported in the original list in the BCMP: Anolis sp., Crocodylus moreletii, and Hemidactylus turcicus. Additionally, we found two species that were not registered on the original list: Dermochelys coriacea and Hemidactylus frenatus. We also updated the name of one species: Cnemidophorus cozumela, which is now recognized as Aspidoscelis cozumela; however, this species only inhabits Cozumel Island. For that reason the whiptail lizard that inhabits Banco Chinchorro BR is Aspidoscelis maslini (Manriquez-Moran et al., 2000; Reeder et al., 2002; Manriquez-Moran et al., 2014). The updated list involves one crocodilian, four marine turtles, two iguanas, two geckos, two anoles, one whiptail lizard, and one snake. In the following paragraphs, we will discuss these results by Order (i.e., Crocodylia, Testudines, and Squamata) with the support of literature on reptiles of the reserve.
Crocodylia--Only one species occurs in the reserve: Crocodylus acutus (American crocodile; Charruau, 2003; Charruau et al., 2005, 2010b, 2012; Charruau and Henaut, 2012). Although C. moreletii had been reported previously (Aguilar-Perera and Aguilar-Davila, 1993), we found no evidence of its presence. It is unlikely that C. moreletii is a permanent resident of this area because it is primarily a freshwater crocodile, and, although the species has salt excretory glands and can tolerate brackish water >20 ppt (Taplin et al., 1985; Escobedo-Gahan et al., 2008), it is very improbable that the species could survive in the hypersaline lagoons (30-65 ppt) of Banco Chinchorro (Charruau et al., 2005). It is possible that the observation of C. moreletii by Aguilar-Perera and Aguilar-Davila (1993) results from an error in distinguishing between these morphologically similar, and sometimes sympatric, species of crocodiles. Several morphological differences exist between C. acutus and C. moreletii, but it can be difficult to distinguish them, even for professional herpetologists (Platt and Rainwater, 2006). Furthermore, C. moreletii and C. acutus interbreed and hybrids are fertile (Machkour-M'Rabet et al., 2009). However, the population of C. acutus in Banco Chinchorro appears to be genetically pure (Machkour-M'Rabet et al., 2009), which would support the absence of C. moreletii in the reserve.
At Banco Chinchorro, C. acutus has been hunted for its skin for several decades as an additional complementary income for fishermen (Solis-Ramirez, 1966; Miller, 1982; Charruau et al., 2005; Colli-Orozco, pers. comm.). However, the hunting at Cayo Centro was not as intense as on the continent, and the cay is now the home of a relatively important and well-conserved population, which has been the subject of many studies since 2003 (population status: Charruau et al., 2005; population genetics: Cedeno-Vazquez et al., 2008; Machkour-M'rabet et al., 2009; growth rates: Charruau et al., 2010b; nesting ecology: Charruau et al., 2010a; bacterial flora: Perez-Flores et al., 2011; age estimation: Charruau, 2011, 2012; maternal behavior: Charruau and Henaut, 2012; Charruau et al., 2012; toxicology: Charruau et al., 2013). All of these studies indicate a stable and healthy reproductive, genetic, and population status for C. acutus and support that Banco Chinchorro BR is an important refuge for the species in the Yucatan Peninsula.
Testudines--Four species of sea turtles are known to be present at Banco Chinchorro: Caretta caretta, Chelonia mydas, Eretmochelys imbricata, and Dermochelys coriacea. In the original species list of the BCMP, three marine turtles were included: Caretta caretta (loggerhead sea turtle), Chelonia mydas (green turtle), and Eretmochelys imbricata (hawksbill sea turtle), all of which are from the Cheloniidae family (INE, 2000). These three species were observed at the reserve by Herrera-Pavon (1991), fishermen, and the reserve staff. The first author also observed several individuals of Eretmochelys imbricata in the reef lagoon. Furthermore, Herrera-Pavon (2001) reported a fourth species of marine turtle, Dermochelys coriacea (leatherback sea turtle), after having observed tracks of this species on the beach of Cayo Norte Mayor (Herrera-Pavon, 2001). This author also told us about the capture of one Dermochelys coriacea and observation of a few individuals in the reserve (Herrera-Pavon, pers. comm.). Thus, we included this fourth species of marine turtle on the list. Little is known about sea turtles at Banco Chinchorro, but the reserve seems to be an important feeding, reproductive, and nesting area for these species (Herrera-Pavon, 1991, 2001).
Before the establishment of the permanent ban on fishing or capture of all marine turtle species in Mexico (Secretaria de Medio Ambiente y Recursos Naturales [SEMARNAT] in Diario Oficial de la Federacion 1990), turtles were fished or captured on beaches of Cayo Lobos and Cayo Norte during the nesting season by "Turtlers" (i.e., turtle-hunters) coming from Cozumel Island, Xcalak (a small village on the southern coast of Quintana Roo), and Belize (Miller, 1982). In fact, according to Miller (1982), prior to the late 1960s, trips of fishermen to Banco Chinchorro were sporadic and principally were made to capture the sea turtle E. imbricata and crocodiles (referred as "alligators" in the text).
Herrera-Pavon (2001) reported the nesting of Caretta caretta and Eretmochelys imbricata at Cayo Lobos and Cayo Norte Mayor, and observed tracks of Chelonia mydas and Dermochelys coriacea on the beach of Cayo Lobos and Cayo Norte Mayor, respectively, which would suggest a sporadic nesting of these species in the reserve. We also observed nests of Caretta caretta at Cayo Centro. Although turtle nests can be observed at Cayo Centro and Cayo Norte Mayor, Cayo Lobos appears to be the preferred nesting area by turtles at Banco Chinchorro. According to Herrera-Pavon (2001), this could be due to its close location to the coral reef breaker zone, its sparse vegetation, and its proximity to beaches with easy access. Banco Chinchorro is likely a feeding area for the four species.
Squamata--With regard to geckos, we observed Hemidactylus frenatus (house gecko), which is a species not listed in the BCMP. Additionally, Hemidactylus turcicus appeared to be misspelled (i.e., Hemidactylus tursicus) in the BCMP (INE, 2000) as reported by Castillo et al., (in litt.). However, H. turcicus has not been reported along the east coast of the peninsula, where H. frenatus is present (Lee, 1996; Kohler, 2008). We can consider that the report of H. turcicus in the reserve may have been a misidentification of H. frenatus because of the morphological similarity between the two species. Moreover, the specimen of H. turcicus deposited in 2010 at the collection of ECOSUR was later identified as H. frenatus. Hemidactylus frenatus is a small, oviparous, nocturnal gecko and an invasive species native to South Asia, which has been introduced worldwide (Case et al., 1994; Caicedo-Portilla and Dulcey-Cala, 2011). Hemidactylus frenatus may have been introduced in Mexico through Acapulco harbor in Guerrero state by commercial boats and then spread to other states (Valdez-Villavicencio and Peralta-Garcia, 2008). The species was first reported in Quintana Roo in 1996 (Schmidt-Ballardo et al., 1996) but likely arrived in this state in the early 1980s (Lee, 1996). Because H. frenatus is strongly associated with developed areas, its arrival to the atoll almost certainly occurred through human means, hidden in material or food brought by fishermen to the atoll during the 1980s.
The only other species of gecko identified at Banco Chinchorro was Aristelliger georgeensis, the St. George Island gecko. This is a large, nocturnal, oviparous gecko principally occurring in offshore islands of Quintana Roo, Belize, Honduras, and scattered throughout mainland coastal localities of Quintana Roo and Belize (Lee, 1996; Kohler, 2008). This species reaches 115 mm SVL (Lee, 1996), but the largest specimen captured at Banco Chinchorro was an adult male 84 mm SVL from Cayo Centro.
Ctenosaura similis and Iguana iguana, the black and green iguanas, are the biggest terrestrial lizards on the reserve and are very abundant at Cayo Centro and Cayo Norte Mayor. At Cayo Centro they are abundant around the field station and fishermen camps. Color patterns of both species are similar to the pattern described by Lee (1996).
We also identified two species of anoles: Anolis allisoni and Anolis sagrei. Anolis allisoni, the Allison's anole, is a trunk-crown anole (Losos, 2009) and was first reported in Banco Chinchorro by Nieto-Montes de Oca et al. (1999). This insular species also occurs on Lighthouse Atoll in Belize, in Bay Islands and Cayos Cochinos in Honduras, and in Cuba (Schmidt, 1941; Ruibal and Williams, 1961; Platt et al., 1999). Anolis sagrei, the brown anole, is a trunk-ground anole (Losos, 2009) native to Cuba, the Bahamas, and Jamaica; and it has been introduced to many Caribbean countries and islands, including the Yucatan Peninsula, where it is widespread in coastal areas (Lee, 1996; Kohler, 2008).
The BCMP mentioned a third and undetermined species of anole (Anolis sp INE, 2000), which we never captured or observed during our visits to Banco Chinchorro BR. Moreover, the two specimens identified as Anolis lemurinus from Banco Chinchorro deposited in the reptile collection of ECOSUR are neonates of A. sagrei. Thus no A. lemurinus have been identified at Banco Chinchorro BR.
The last species of lizard identified in the reserve is Aspidoscelis maslini, the Maslin's whiptail. This species was not listed in the BCMP but another species of Aspidoscelis was listed with the former genus name Cnemidophorus. This species, Cnemidophorus cozumela, has been included into the genus Aspidoscelis as the Aspidoscelis cozumela complex with three recognized species: Aspidoscelis rodecki, A. cozumela, and A. maslini (Reeder et al., 2002). The species present at Banco Chinchorro is A. maslini, (Taylor and Cooley, 1995; Manriquez-Moran et al., 2000). Aspidoscelis maslini has the widest distribution of any parthenogenetic species of the group in the Yucatan Peninsula. This species inhabits mainly the halophyte vegetation of the beaches, but some populations occur far from the coasts in tropical rainforests (Lee, 1996). Aspidoscelis maslini reproduces by parthenogenesis, whereby all the individuals are female and genetically identical (Moritz et al., 1992; Manriquez-Moran et al., 2000; Manriquez-Moran, 2002). These ground-dwelling lizards are very dependent on environmental temperatures; and, although they have a high capacity of thermoregulation, their activity drops considerably during cloudy days (Diaz de la Vega-Perez et al., 2013).
Furthermore, in 1998 Castillo et al. (in litt.) reported the presence of the boa (Boa constrictor) in Cayo Centro. We never observed boas during our surveys and no one interviewed has mentioned it. However, recently (March 2015), one individual was captured by GECI and delivered to park rangers. Boas are a successful invasive species (Romero-Najera et al., 2007; Vazquez-Dominguez et al., 2012; Reynolds et al., 2013), and their presence would likely be evident in the reserve if a resident population were present. However, PC has never observed a boa in 11 years of work on the reserve. Moreover, reserve staff and fishermen who work year-round in the reserve have never observed boas. Thus, because no boas have been observed in the reserve from the report of Castillo et al. (in litt.), from 1998 to 2015, we consider that a population of this species is likely not present at Banco Chinchorro BR. However, it is likely that some individuals could arrive occasionally to the reserve by hurricanes or on floating vegetation driven by marine currents; and, although boas can reproduce by facultative parthenogenesis (Booth et al., 2011; Lara-Resendiz et al., 2013), these isolated individuals have likely not established a population in the reserve. A tissue sample was collected from the boa to determinate its genetic affinity with other populations of the region for future studies.
Protection and Conservation Status--There is no monitoring of sea turtle nests at Banco Chinchorro BR, and we strongly recommend the implementation of such monitoring there. Cayo Lobos, the main nesting site of sea turtles at Banco Chinchorro, is the only cay with no human presence, but it is used by illegal fishermen who collect eggs from nests of sea turtles (Reserve staff, pers. comm.).
With the information obtained from this study, Anolis allisoni and Aspidoscelis maslini were included in the list of protected species by Mexican law (Diaz de la Vega-Perez and Charruau, 2013; Diaz de la Vega-Perez and Mendez-de la Cruz, 2013). The Banco Chinchorro BR is a critical protected area for both species. The Banco Chinchorro BR is the only site in Mexico where populations of Anolis allisoni occur (Nieto-Montes de Oca et al., 1999) with a distribution area of almost 5.8 [km.sup.2], representing 0.0003% of the national area. This species is categorized as "subject to special protection" by the NOM-059-ECOL, which will be published (Diaz de la Vega-Perez and Charruau, 2013).
In the case of Aspidoscelis maslini, the organisms inhabiting Banco Chinchorro BR are geographically and genetically isolated from the closest continental population in Mahahual (Manriquez-Moran et al., 2014). Banco Chinchorro provides adequate environmental characteristics for these lizards; their abundance in the reserve is high compared with many continental populations affected by the environmental modifications caused by tourist infrastructure (Diaz de la Vega-Perez et al., 2013). Aspidoscelis maslini after this study is categorized as "threatened" by the Mexican biodiversity protection law, NOM-059-ECOL (Diaz de la Vega-Perez and Mendez-de la Cruz, 2013).
Anolis sagrei and Hemidactylus frenatus have no protection or conservation status (Table 2). Anolis sagrei is the most abundant and widespread species of the Caribbean anoles (Schoener and Schoener, 1980; Losos et al., 1993) and has colonized or been introduced in many countries (or islands) of this region, but also in other parts of the world, such as Taiwan (Norval et al., 2002) and Hawaii (Goldberg et al., 2002). As an introduced species, it can be a threat to autochthonous lizard species by competing for resources or by consuming smaller lizard species (Campbell, 1999; Echternacht, 1999; Gerber and Echternacht, 2000). However, A. sagrei has likely been established at Banco Chinchorro BR for a long time, and our observations do not suggest that this species is a threat to other species.
Hemidactylus frenatus has been responsible for the displacement or extinction of several native or introduced lizards (principally geckos) on worldwide islands and continents (Case et al., 1994; Petren and Case, 1996; Cole et al., 2005; Dame and Petren, 2006; Caicedo-Portilla and Dulcey-Cala, 2011). It is a serious threat for Aristelliger georgeensis at Banco Chinchorro, its eradication from Cayo Centro is strongly recommended, and precautions must be taken to prevent its spread to Cayo Norte.
The black rat and the feral cat (Felis catus) are also present at Cayo Centro and Cayo Norte, respectively (Charruau, 2003). These invasive species are a serious threat to reptile populations, especially to lizards. Fortunately, a program of rat and cat eradication is currently ongoing at Banco Chinchorro. The removal or control of the exotic coconut palm is also recommended because it displaces and replaces native vegetation and serves as a refuge for rats.
Moreover, reptile habitat at Banco Chinchorro BR has been severely damaged by the passage of tropical cyclones in recent years, beginning with Hurricane Dean, which directly struck the cays of Banco Chinchorro in 2007 (Charruau et al., 2010a). Since that time, coastal dune vegetation and black mangrove (Avicenia germinans) forest are recovering rapidly, while red mangrove (Rhizophora mangle) recovery has been slow. A restoration program of the red mangrove fringe at Banco Chinchorro has been implemented and its total recovery could take several decades. Quintana Roo is the Mexican state with the highest frequency of tropical cyclones of all intensity categories (INE, 2000), and the frequency of higher category hurricanes is expected to increase in the future due to global warming (Knutson et al., 2010). During recent decades, the frequency of major hurricanes of category 3, 4, and 5 increased at Banco Chinchorro, while frequency of hurricanes of category 1 and 2 decreased (Charruau, 2010). This increase in major hurricane occurrence at Banco Chinchorro could be a threat to the reptiles of the reserve. Thus, studies on effects of tropical cyclones on reptile species at Banco Chinchorro must be undertaken in the future.
Finally, nonintroduced reptiles from Banco Chinchorro are candidates for consideration as Evolutionary Significant Units (ESU). Although several definitions for ESUs have been developed since its original formulation (Fraser and Bernatchez, 2002), three criteria can be used to define an ESU: a current geographical separation, a high degree of genetic differentiation, and locally adapted phenotypic traits. In Banco Chinchorro, populations of terrestrial reptiles are completely separated from the continent, which suggests a very low gene flow between them and continental populations. In the case of crocodiles, although they can swim long distances in open ocean (Groombridge, 1987), Machkour-M'rabet et al. (2009) revealed a high genetic differentiation among populations of Crocodylus acutus along the coast of Quintana Roo. Thus, we might expect greater genetic differentiation from other reptile species (with the exception of sea turtles) justified by the fact that they presumably have lower capabilities to disperse between Banco Chinchorro and the continent than crocodiles. Populations of Aspidoscelis maslini in the Yucatan Peninsula, composed of clonal organisms, are geographically and genetically separated, and the population inhabiting Banco Chinchorro BR could represent specific ecological and physiological characteristics, implying that each clonal population could be considered as an ESU. Nevertheless, other species could strongly differ from the continental populations because of isolation; therefore, we strongly recommend studies comparing the behavior, physiology, and ecology of the mainland and island populations to better understand their evolution (Losos et al., 1997; Losos and Ricklefs, 2009; Diaz de la Vega-Perez et al., 2013; Siliceo-Cantero and Garcia, 2014). The isolation of reptile populations from Banco Chinchorro, the reduced area in the island, and the specialized environmental conditions on the island (e.g., high salinity with no freshwater source, lower resource diversity) may lead to local adaptation. Taken together, several populations of reptiles at Banco Chinchorro may be considered ESUs. However, genetic and phenotypic studies are necessary to accurately identify ESUs on the reserve.
We are grateful to E. Colin Guzman and two anonymous reviewers for the comments that helped to improve the manuscript. We also thank S. Larocque-Desroches for the English review and H. Weissenberger for the map elaboration. We thank Banco Chinchorro Biosphere Reserve (CONANP) and its staff for their assistance and support during field work. This study was funded by the Consejo Nacional de Ciencia y Tecnologia (scholarship 165067 to AHDVP) and by the Universidad Nacional Autonoma de Mexico (PAPIIT IN215011). PC. was awarded with a fellowship from the postdoctoral fellowship program of the Universidad Nacional Autonoma de Mexico. Scientific research permits were issued by the Secretaria de Medio Ambiente y Recursos Naturales (SEMARNAT) of Mexico (Oficios SGPA/DGVS 03366/12, SGPA/DGVS 04528/11 y SGPA/DGVS 08305/11).
AGUILAR-PERERA, A., AND W. AGUILAR-DAVILA. 1993. Banco Chinchorro: Arrecife coralino en el Caribe. Pages 807-816 in Biodiversidad marina y costera de Mexico (S. I., Salazar-Vallejo and N. E. Gonzalez, editors). Comision Nacional para el Conocimiento y Aprovechamiento de la Biodiversidad and Centro de Investigaciones de Quintana Roo, Mexico.
ARDISSON, P. L., M. A. MAY-KU, M. T. HERRERA-DORANTES, AND A. ARELLANO-GUILLERMO. 2011. El sistema arrecifal mesoamerica no-Mexico: consideraciones para su designation como zona maritima especialmente sensible. Hidrobiologica 21:261280.
BICKFORD, D., S. D. HOWARD, D. J. J. NG, AND J. A. SHERIDAN. 2010. Impacts of climate change on the amphibians and reptiles of Southeast Asia. Biodiversity and Conservation 19:1043-1062.
BOOTH, W., D. H. JOHNSON, S. MOORE, C. SCHAL, AND E. L. VARGO. 2011. Evidence for viable, non-clonal but fatherless Boa constrictor. Biology Letters 7:253-256.
CAICEDO-PORTILLA, R., AND C. J. DULCEY-CALA. 2011. Distribution del gecko introducido Hemidactylus frenatus (Dumeril y Bribon 1836) (Squamata: Gekkonidae) en Colombia. Biota Colombiana 12:46-56.
CAMPBELL, T. S. 1999. Consequences of the Cuban brown anole invasion: it's not easy being green. Anolis Newsletter V:12-21.
CASE, T. J., D. T. BOLGER, AND K. PETREN. 1994. Invasions and competitive displacement among house geckos in the tropical Pacific. Ecology 75:464-477.
CEDENO-VAZQUEZ, J. R., D. RODRIGUEZ, S. CALME, J. P. ROSS, L. D. DENSMORE III, AND J. B. THORBJARNARSON. 2008. Hybridization between Crocodylus acutus and Crocodylus moreletii in the Yucatan Peninsula: I. evidence from mitochondrial DNA and morphology. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 309A:661-673.
CHARRUAU, P. 2003. Management of terrestrial systems of Banco Chinchorro Biosphere Reserve, Quintana Roo, Mexico. Memoire de DESS, Institut d'Ecologie Appliquee, Universite Catholique de l'Ouest, Angers, France.
CHARRUAU, P. 2010. Ecologia y etologia de anidacion del cocodrilo americano (Crocodylus acutus): un estudio para su conservation. Tesis de Doctorado, El Colegio de la Frontera Sur, Chetumal, Quintana Roo, Meixico.
CHARRUAU, P. 2011. Estimation de la edad de los cocodrilos (Crocodylus acutus) de Banco Chinchorro, Quintana Roo, Mexico. Quehacer Cientifico en Chiapas 1:36-43.
CHARRUAU, P. 2012. Microclimate of American crocodile nests in Banco Chinchorro Biosphere reserve, Mexico: effect on incubation length, embryos survival and hatchlings sex. Journal of Thermal Biology 37:6-14.
CHARRUAU, P., AND Y. HENAUT. 2012. Nest attendance and hatchling care in wild American crocodiles (Crocodylus acutus) in Quintana Roo, Mexico. Animal Biology 62:29-51.
CHARRUAU, P., J. R. CEDENO-VAZQUEZ, AND S. CALME. 2005. Status and conservation of the American crocodile (Crocodylus acutus) in Banco Chinchorro Biosphere Reserve, Quintana Roo, Mexico. Herpetological Review 36:390-395.
CHARRUAU, P., J. R. CEDENO-VAZQUEZ, AND G. KOHLER. 2015. Amphibians and reptiles of the Yucatan Peninsula. Pages 257-293 in Biodiversity and conservation of the Yucatan Peninsula (G. Islebe, S. Calme, B. Schmook, and J. L. Leon-Cortes, editors). Springer International Publishing, Switzerland.
CHARRUAU, P., Y. HENAUT, AND T. LEGORETA. 2013. Organochlorine pesticides in nest substratum and infertile eggs of American crocodiles (Reptilia, Crocodylidae) in a Mexican Caribbean atoll. Caribbean Journal of Science 47:1-12.
CHARRUAU, P., J. B. THORBJARNARSON, AND Y. HENAUT. 2010a. Tropical cyclones and reproductive ecology of Crocodylus acutus Cuvier, 1807 (Reptilia: Crocodilia: Crocodylidae) on a Caribbean atoll in Mexico. Journal of Natural History 44:741761.
CHARRUAU, P., J. R. CEDENO-VAZQUEZ, A. VILLEGAS, AND H. GONZALEZ CORTES. 2010b. Tasas de crecimiento del cocodrilo americano (Crocodylus acutus) en estado silvestre en la Peninsula de Yucatan, Mexico. Revista Latinoamericana de Conservation 1:63-72.
CHARRUAU, P., J. PEREZ-FLORES, J. G. PEREZ-JUAREZ, J. R. CEDENO-VAZQUEZ, AND R. ROSAS-CARMONA. 2012. Oral and cloacal microflora of wild crocodiles Crocodylus acutus and C. moreletii in the Mexican Caribbean. Diseases of Aquatic organisms 98:27-39.
COLE, N. C., C. G. JONES, AND S. HARRIS. 2005. The need for enemy-free space: the impact of an invasive gecko on island endemics. Biological Conservation 125:467-474.
CONVENTION ON INTERNATIONAL TRADE IN ENDANGERED SPECIES OF WILD FAUNA AND FLORA [CITES]. 2015. Convention text, Appendices I, II, III. Available at: https://www.cites.org/ eng/disc/text.php. Accessed 14 December 2015 .Dame, E. A., and K Petren. 2006. Behavioral mechanisms of invasion and displacement in Pacific island geckos (Hemidactylus). Animal Behavior 71:1165-1173.
DIAZ DE LA VEGA-PEREZ, A. H., AND P. CHARRUAU. 2013. Evaluation del riesgo de extincioi n de Anolis allisoni, de acuerdo al numeral 5.7 de la Norma Oficial Mexicana 059-SEMARNAT2010 y propuesta para la inclusion de la especie. SEMARNAT, Ciudad de Meixico, Meixico.
DIAZ DE LA VEGA-PEREZ, A. H., AND F. R. MENDEZ-DE LA CRUZ. 2013. Evaluacioi n del riesgo de extincioi n de Aspidoscelis maslini de acuerdo al numeral 5.7 de la Norma Oficial Mexicana 059SEMARNAT-2010 y propuesta para la inclusion de la especie. SEMARNAT, Ciudad de Mexico, Mexico.
DIAZ DE LA VEGA-PEREZ, A. H., P. CHARRUAU, AND I. SAAVEDRA-VALERO. 2014. Anolis sagrei (Brown Anole). Abscess. Herpetological Review 45:491.
DIAZ DE LA VEGA-PEREZ, A. H., V. H. JIMENEZ-ARCOS, N. L. MANRIQUEZ-MORAN, AND F. R. MENDEZ-DE LA CRUZ. 2013. Conservatism of thermal preferences between parthenogenetic Aspidoscelis cozumela complex (Squamata:Teiidae) and their parental species. Herpetological Journal 23:93-104.
ECHTERNACHT, A. C. 1999. Possible causes for the rapid decline in population density of green anoles, Anolis carolinensis (Sauria: Polychrotidae) following invasion by the brown anole, Anolis sagrei, in the southeastern United States. Anolis Newsletter V:22-27.
ESCOBEDO-GALVAN, A. H., V. PALACIOS-CHAVEZ, AND A. VOVIDESTEJERA. 2008. Crocodylus moreletii (Morelet's crocodile). Salinity tolerance. Herpetological Review 39:346-347.
FIGUEROA, F., AND V SANCHEZ-CORDERO. 2008. Effectiveness of natural protected areas to prevent land use and land cover change in Mexico. Biodiversity and Conservation 17:32233240.
FITZGERALD, L. A. 2012. Finding and capturing reptiles. Pages 7788 in Reptile biodiversity: standard methods for inventory and monitoring (R. McDiarmid, M. S. Foster, C. Guyer, J. Whitfield Gibbons, and N. Chernoff, editors). University of California Press, Berkeley and Los Angeles.
FLORES-VILLELA, O., AND U. GARCIA VAZQUEZ. 2014. Biodiversidad de reptiles en Mexico. Revista Mexicana de Biodiversidad 85:467-475.
FRASER, D. J., AND L. BERNATCHEZ. 2002. Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology 10:2741-2752.
GERBER, G. P., AND A. C. ECHTERNACHT. 2000. Evidence for asymmetrical intraguild predation between native and introduced Anolis lizards. Oecologia 124:599-607.
GIBBONS, J. W., D. E. SCOTT, J. R. TRAVIS, K. A. BUHLMANN, T. D. TUBERVILLE, B. S. METTS, J. L. GREENE, T. MILLS, Y. LEIDEN, S. POPPY, AND C. T. WINNE. 2000. The global decline of reptiles, deja vu amphibians. BioScience 50:653-666.
GLOBAL ENVIRONMENT OUTLOOK 5. 2012. 5th global environment outlook (GEO-5). United Nations environment programme, Valletta, Malta.
GOLDBERG, S. R., F. KRAUS, AND C. BURSEY. 2002. Reproduction in an introduced population of the brown anole, Anolis sagrei, from O'ahu, Hawai'i. Pacific Science 56:163-168.
GROOMBRIDGE, B. 1987. The distribution and status of world crocodilians. Pages 9-22 in Wildlife management: crocodiles and alligators (G. J. W. Webb, S. C. Manolis, and P. J. Whitehead, editors). Surrey Beatty and Sons Pty Limited, Chipping Norton, Australia.
HERNANDEZ, A., F. A. RODRIGUEZ-ZARAGOZA, M. C. GARCIA, J. M. CASTRO, AND J. MEDINA-FLORES. 2008. El manejo sostenible de los recursos pesqueros de la Reserva de la Biosfera Banco Chinchorro. World Wildlife Fund, Ciudad de Mexico, Mexico.
HERRERA-PAVON, R. L. 1991. Captura incidental de tortugas marinas en la Zona Sur del Estado de Quintana Roo. Tesis de M. En C., Instituto Tecnologico Agropecuario No 16, Chetumal, Quintana Roo, Mexico.
HERRERA-PAVON, R. L. 2001. Anidacion de las tortugas marinas en Banco Chinchorro. Pages 126-128 in Memorias del XI taller regional sobre programas de conservacion de tortugas marinas en la Peninsula de Yucatan (M. Aceves and R. Villavicencia, editors). Riviera Maya, Marzo 2001:8-10.
HUEY, R. B., C. A. DEUTSCH, J. J. TEWKSBURY, L. J. VITT, P. E. HERTZ, H. J. ALVAREZ-PEREZ, AND T. GARLAND, JR. 2009. Why tropical forest lizards are vulnerable to climate warming. Proceedings of the Royal Society 276:1939-1948.
INSTITUTO NACIONAL DE ECOLOGIA [INE]. 2000. Programa de manejo Reserva de la Biosfera Banco Chinchorro, Mexico. Instituto Nacional de Ecologia, Ciudad de Mexico, Distrito Federal, Mexico.
INTERNATIONAL UNION FOR CONSERVATION OF NATURE [IUCN]. 2015. The IUCN red list of threatened species. Version 2015. 4. Available at < http://www.iucn.org/ > Accessed 14 December 2015.
KNUTSON, T. R.,J. L. MCBRIDE, J. CHAN, K. EMANUEL, G. HOLLAND, C. LANDSEA, I. HELD, J. P. KOSSI, A. K. SRIVASTAVA, AND M. SUGI. 2010. Tropical cyclones and climate change. Nature Geoscience 3:157-163.
KOHLER, G. 2008. Reptiles of Central America. Second edition. Herpeton Verlag, Offenbach, Germany.
LANE, M. B. 2001. Affirming new directions in planning theory: comanagement of protected areas. society and Natural Resources: an International Journal 14:657-671.
LARA-RESENDIZ, R. A., B. C. LARRAIN BARRIOS, A. H. DIAZ DE LA VEGAPEREZ, AND E. CENTENERO-ALCALA. 2013. Boa constrictor (Boa constrictor). Reproduction: facultative parthenogenesis. Herpetological Review 44:151-152.
Lee, J. C. 1996. The amphibians and reptiles of the Yucatan Peninsula. Cornell University Press, Ithaca, New York.
LOSOS, J. B. 2009. Lizards in an evolutionary tree, ecology and adaptive radiation of anoles. University of California Press, Berkeley.
LOSOS, J. B., and R. E. Ricklefs (editors). 2009. The theory of island biogeography revisited. Princeton University Press, Princeton, New Jersey.
Losos, J. B., J. C. Marks, and T. W. Schoener. 1993. Habitat use and ecological interactions of an introduced and a native species of Anolis lizard on Grand Cayman, with a review of the outcomes of anole introductions. Oecologia 95:525-532.
LOSOS, J. B., K. I. WARHEIT, AND T. W. SCHOENER. 1997. Adaptative differentiation following experimental island colonization in Anolis lizards. Letters to Nature. 387:70-73.
MACHKOUR-M'RABET, S., Y. HENAUT, P. CHARRUAU, M. GEVREY, P. WINTERTON, AND L. LEGAL. 2009. Between introgression events and fragmentation, islands are the last refuge for the American crocodile in Caribbean Mexico. Marine Biology 156:1321-1333.
MANRIQUEZ-MORAN, N. L. 2002. Origen y diversidad clonal en las especies de lagartijas partenogeneticas del complejo Cnemidophorus cozumela (Reptilia: Teiidae). Tesis de doctorado, Instituto de Biologia, Universidad Nacional Autonoma de Mexico, Ciudad de Mexico, Distrito Federal, Mexico.
MANRIQUEZ-MORAN, N. L., F. R. MENDEZ-DE LA CRUZ, AND R. W. MURPHY. 2014. Genetic variation and origin of parthenogenesis in the Aspidoscelis cozumela complex: evidence from mitochondrial genes. Zoological Science 31:14-19.
MANRIQUEZ-MORAN, N. L., M. VILLAGRAN-SANTA CRUZ, AND F. R. MENDEZ-DE LA CRUZ. 2000. Origin and evolution of the parthenogenetic lizards, Cnemidophorus maslini and C. cozumela. Journal of Herpetology 34:634-637.
MILLER, D. L. 1982. Mexico's Caribbean fishery: recent change and current issues. Ph.D. dissertation, The University of Wisconsin, Milwaukee.
MORITZ, C., J. W. WRIGHT, V. SINGH, AND W. M. BROWN. 1992. Mitochondrial DNA analyses and the origin and relative age of parthenogenetic Cnemidophorus. V. The cozumela species group. Herpetologica 48:417-424.
MURPHY, R. W., AND F. R. MENDEZ-DE LA CRUZ. 2010. The herpetofauna of Baja California and its associated islands. Pages 239-273 in A conservation assessment and priorities (L. D. Wilson, J. H. Townsend, and J. D. Johnson, editors). Eagle Mountain Publishing, Eagle Mountain, Utah.
MYERS, N., R. A. MITTERMEIER, C. G. MITTTERMEIER, G. A. B. DA FONSECA, AND J. KENT. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-858.
NIETO-MONTES DE OCA, A., H. BAHENA-BASAVE, AND F. R. MENDEZ-DE LA CRUZ. 1999. Anolis allisoni (Allison's anole). Herpetological Review 30:233.
NORVAL, G., J. MASO, H. CHU, AND L. CHEN. 2002. A new record of an introduced species, the brown anole (Anolis sagrei) (Dumeril and Bibron, 1837), in Taiwan. Zoological Studies 41:332-336.
PEREZ-FLORES, J., P. CHARRUAU, AND J. G. PEREZ-JUAREZ. 2011. Bacterial isolation from wound and fibriscess in wild American crocodiles (Crocodylus acutus) of Banco Chinchorro. Crocodile Specialist Group Newsletter 30:20-22.
PETREN, K., AND T. J. CASE. 1996. An experimental demonstration of exploitation competition in an ongoing invasion. Ecology 77:118-132.
PLATT, S. G., AND T. A. RAINWATER. 2006. A review of morphological characters useful for distinguishing Morelet's crocodile (Crocodylus moreletii) and American crocodile (Crocodylus acutus) with an emphasis on populations in the coastal zone of Belize. Bulletin of the Chicago Herpetological Society 40:25-29.
PLATT, S. G., J. C. MEERMAN, AND T. R. RAINWATER. 1999. Diversity, observations, and conservation of the herpetofauna of Turneffe, Lighthouse, and Glovers atolls, Belize. British Herpetological Society Bulletin 66:1-13.
REEDER, T. W., C. J. COLE, AND H. C. DESSAUER. 2002. Phylogenetic relationships of whiptail lizards of the genus Cnemidophorus (Squamata: Teiidae): a test of monophyly, reevaluation of karyotypic evolution, and a review of hybrid origins. American Museum Novitates 3365:1-61.
REYNOLDS, R. G., A. R. PUENTE-ROLON, N. REED, AND L. J. REVELL. 2013. Genetic analysis of a novel invasion of Puerto Rico by an exotic constricting snake. Biological Invasions 15:953-959.
ROMERO-NAJERA, I., A. D. CUARON, AND C. GONZALEZ-BACA. 2007. Distribution, abundance, and habitat use of introduced Boa constrictor threatening the native biota of Cozumel Island, Mexico. Biodiversity and Conservation 16:1183-1195.
RUIBAL, R., AND E. E. WILLIAMS. 1961. Two sympatric Cuban anoles of the Carolinensis group. Bulletin of the Museum of Comparative Zoology 125:181-208.
SCHMIDT, K. P. 1941. The amphibians and reptiles of British Honduras. Field Museum of Natural History, Zoological Series 22:475-510.
SCHMIDT-BALLARDO, W., F. MENDOZA-QUIJANO, AND MA. E. MARTINEZSOLIS. 1996. Range extensions for Hemidactylus frenatus in Mexico. Herpetological Review 27:40.
SCHOENER, T. W., AND A. SCHOENER. 1980. Densities, sex ratios, and population structure in four species of Bahamian Anolis lizards. Journal of Animal Ecology 49:19-53.
SECRETARIA DE MEDIO AMBIENTE Y RECURSOS NATURALES [SEMARNAT]. 1990. Acuerdo por el que se establece veda total para todas las especies y subespecies de tortugas marinas en aguas de jurisdiction nacional de los litorales del Oceano Pacifico, Golfo de Mexico y Mar Caribe. Diario Oficial de la Federation, Mexico, Mayo 31, 1990:21-22.
SECRETARIA DE MEDIO AMBIENTE Y RECURSOS NATURALES [SEMARNAT]. 1996. Decreto por el que se declara area natural protegida, con el caracter de Reserva de la Biosfera, la region conocida como Banco Chinchorro, ubicada frente a las costas del Municipio de Othon P. Blanco, Estado de Quintana Roo, con una superficie total de 144,360-00-00 hectareas. Diario Oficial de la Federation, Mexico, Julio 19, 1996:7-10.
SECRETARIA DE MEDIO AMBIENTE Y RECURSOS NATURALES [SEMARNAT]. 2010. Norma Oficial Mexicana N0M-059-SEMARNAT2010, Protection ambiental-especies nativas de Mexico de flora y fauna silvestres-categorias de riesgo y especificaciones para su inclusion, exclusion o cambio-lista de especies en riesgo. Diario Oficial de la Federation, Mexico, Diciembre 2010:1-78.
SILICEO-CANTERO, H. H., AND A. GARCIA. 2014. Actividad y uso del habitat de una poblacion insular y una continental de lagartijas Anolis nebulosus (Squamata: Polychrotidae) en un ambiente estacional. Revista Mexicana de Biodiversidad 86 (2015):406-411.
SINERVO, B., F. MENDEZ-DE LA CRUZ, D. B. MILES, B. HEULIN, E. BASTIAANS, M. VILLAGRAN-SANTA CRUZ, R. LARA-RESENDIZ, N. MARTINEZ-MENDEZ, M. L. CALDERON-ESPINOSA, R. MEZA-LAZARO, H. GADSDEN, L. J. AVILA, M. MORANDO, I. J. DE LA RIVA, P. V. SEPULVEDA, C. F. DUARTE ROCHA, N. IBARGUENGOYTIA, C. AGUILAR PUNTRIANO, M. MASSOT, V. LEPETZ, T. A. OKSANEN, D. G. CHAPPLE, A. M. BAUER, W. R. BRANCH, J. CLOBERT, AND J. W. SITES, JR. 2010. Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894-899.
SOLIS-RAMIREZ, M. J. 1966. Recursos pesqueros del territorio de Quintana Roo, Mexico. I. Xcalak y Banco Chinchorro. Trabajos de divulgation Vol. XI, numero 101. Contribution de Instituto Nacional de Investigaciones Biologico-Pesqueras, Secretaria de Industria y Comercio, Direction General de Pesca, Ciudad de Mexico, Mexico.
TAPLIN, L. E., G. C. GRIGG, AND L. BEARD. 1985. Salt gland function in fresh water crocodiles: evidence for a marine phase in Eusuchian evolution? Pages 403-410 in Biology of Australasian frogs and reptiles (G. Grigg, R. Shine, and H. Ehmann, editors). Surrey Beatty and Sons Pty Ltd, Chipping Norton, New South Wales, Australia.
TAYLOR, H. L., AND C. R. COOLEY. 1995. A multivariate analysis of morphological variation among parthenogenetic teiid lizards of the Cnemidophorus cozumela complex. Herpetologica 51:6776.
United Nations Environment Programme/International Union for Conservation of Nature [UNEP/IUCN]. 1988. Coral reefs of the world. Volume 1. Atlantic and Eastern Pacific. UNEP regional seas directories and bibliographies. iuCN, Gland, Switzerland; and Cambridge, England, United Kingdom/ UNEP, Nairobi, Kenya.
VALDEZ-VILLAVICENCIO, J. H., AND A. PERALTA-GARCIA. 2008. Hemidactylus frenatus (Sauria: Gekkonidae) en el noroeste de Mexico. Acta Zoologica Mexicana (nueva serie) 24:229-230.
VAZQUEZ-DOMINGUEZ, E., M. SUAREZ-ATILANO, W. BOOTH, C. GONZALEZ-BACA, AND A. D. CUARON. 2012. Genetic evidence of a recent successful colonization of introduced species on islands: Boa constrictor imperator on Cozumel Island. Biological Invasions 14:2101-2116.
WILSON, L. D., AND J. J. JOHNSON. 2010. Distributional patterns of the herpetofauna of Mesoamerica, a biodiversity hotspot. Pages 30-235 in Conservation of Mesoamerican amphibians and reptiles (L. D. Wilson, J. H. Townsend, and J. J. Johnson, editors). Eagle Mountain Publishing, Eagle Mountain, Utah.
WILSON, L. D., V. MATA-SILVA, AND J. D. JOHNSON. 2013. A conservation reassessment of reptiles of Mexico based on the EVS measure. Amphibian and Reptile Conservation 7:114.
Submitted 28 April 2015.
Acceptance recommended by Associate Editor, Felipe de Jesus Rodriguez Romero, 7 September 2015.
PIERRE CHARRUAU, ANIBAL H. DIAZ DE LA VEGA PEREZ, * AND FAUSTO R. MENDEZ DE LA CRUZ
Centro del Cambio Global y la Sustentabilidad en el Sureste A.C., Calle Centenario del Instituto Juarez s/n, C.P. 86080, Villahermosa, Tabasco, Mexico (PC)
Consejo Nacional de Ciencia y Tecnologea Research Fellow-Centro Tlaxcala de Biologia de la Conducta, Universidad Autonoma de Tlaxcala. Calle del Bosque s/n, C.P. 90000, Tlaxcala Centro, Tlaxcala, Mexico (ADVP)
Laboratorio de Herpetologia, Departamento de Zoologia, Instituto de Biologia, Universidad Nacional Autonoma de Mexico, Ciudad
Universitaria, C.P. 04510, Coyoacan, Distrito Federal, Mexico (FRMC)
* Correspondent: email@example.com
TABLE 1--Terrestrial vegetation associations present in the islands of Banco Chinchorro Biosphere Reserve, Quintana Roo, Mexico. Type Association Cayo Halophyte or coastal Pioneer vegetation Norte and Centro dune vegetation Coastal brush with Lobos Tournefortia gnaphalodes, Ipomoea alba, and Ipomoea pes-caprae Coastal brush with Centro Pithecellobium keyense Low coastal forest with Norte and Centro Bursera simaruba Secondary vegetation Norte and Centro Mangrove Fringe mangrove with Norte and Centro Rhizophora mangle Mixed mangrove with Avicenia Norte and Centro germinans, Conocarpus erectus, Laguncularia racemosa, and Rhizophora mangle Mangrove with Avicenia Norte and Centro germinans Mangrove with Conocarpus Centro erectus TABLE 2--List of reptile species present in Banco Chinchorro Biosphere Reserve, Quintana Roo, Mexico. International Union for Conservation of Nature 2015 (IUCN, http://www-iucn-org/)-Secretaria de Medio Ambiente y Recursos Naturales [SEMARNAT]. 2010. Norma Oficial Mexicana NOM-059-SEMARNAT-2010 * Invasive species.--Indicates no category. Order/Family/Species Spanish and/or English common names Crocodilia Crocodylidae Crocodylus acutus Cocodrilo americano, cocodrilo de rio, American crocodile Testudines Cheloniidae Caretta caretta Tortuga caguama, loggerhead sea turtle Chelonia mydas Tortuga blanca, green turtle Eretmochelys imbricata Tortuga carey, hawksbill sea turtle Dermochelydae Dermochelys coriacea Tortuga laud, leatherback sea turtle Squamata Gekkonidae Aristelliger georgeensis Gecko pestanudo, salamanquesa, St. George Island gecko Hemidactylus frenatus * Gecko, cuija, house gecko Iguanidae Ctenosaura similis Iguana gris, garrobo, iguana rayada, black iguana, common spiny-tailed iguana Iguana iguana Iguana verde, green iguana Dactyloidae Anolis allisoni Lagartija, anolis, Allison's anole Anolis sagrei Lagartija chipojo, brown anole Teiidae Aspidoscelis maslini Lagartija, Picasol, Maslin's whiptail Boidae Boa constrictor Boa Order/Family/Species IUCN CITES 2012 NOM-059 2012 (a) ECOL-2010 (a) Crocodilia Crocodylidae Crocodylus acutus vu Appendix I Pr Testudines Cheloniidae Caretta caretta EN Appendix I P Chelonia mydas EN Appendix I P Eretmochelys imbricata CR Appendix I P Dermochelydae Dermochelys coriacea CR Appendix I P Squamata Gekkonidae Aristelliger georgeensis -- -- Pr Hemidactylus frenatus * -- -- -- Iguanidae Ctenosaura similis LC -- A Iguana iguana -- Appendix II Pr Dactyloidae Anolis allisoni -- -- -- Anolis sagrei -- -- -- Teiidae Aspidoscelis maslini LC -- -- Boidae Boa constrictor -- Appendix II A Order/Family/Species Reproduction-sex Source determination (c) modes (b) Crocodilia Crocodylidae Crocodylus acutus Ovi-TSD 1,2,3,-4 Testudines Cheloniidae Caretta caretta Ovi-TSD 1,2,3 Chelonia mydas Ovi-TSD 2,3 Eretmochelys imbricata Ovi-TSD 1,2,3 Dermochelydae Dermochelys coriacea Ovi-TSD 2,3 Squamata Gekkonidae Aristelliger georgeensis Ovi-Chrom 1,2,3,4 Hemidactylus frenatus * Ovi-Chrom 1 Iguanidae Ctenosaura similis Ovi-Chrom 1,2,3 Iguana iguana Ovi-Chrom 1,2,3 Dactyloidae Anolis allisoni Ovi-Chrom 1,2,3,4 Anolis sagrei Ovi-Chrom 1,3 Teiidae Aspidoscelis maslini Ovi-Parth 1,2,3 Boidae Boa constrictor Viv-FP 1,3 (a) VU: vulnerable; EN: endangered; CR: critically endangered; LC: least concern; P: in danger of extinction; A: threatened; Pr: subject to special protection. (b) Ovi: oviparous; Viv: Viviparous; TSD: Temperature-dependent Sex Determination; Chrom: Chromosomal; Parth: Parthenogenetic; FP: Facultative parthenogenetic. (c) 1: survey; 2: interview; 3: literature including MPBC; 4: museum specimen. TABLE 3--Voucher specimens from Banco Chinchorro Bio-sphere Reserve in the reptile collections at Museo de Zoologia of El Colegio de la Frontera Sur-Chetumal (ECO-CH-H) and at the Facultad de Ciencias-Universidad Nacional Autonoma de Mexico (MZFC).--Indicates no data. Species Vouchers Year collected Crocodylus acutus ECO-CH-H 2733 -- Aristelliger georgeensis ECO-CH-H 2788-2789 2011 MZFC 10653 1999 Hemidactylus frenatus ECO-CH-H 2790-2791 2011 ECO-CH-H 2786a 2010 Anolis allisoni ECO-CH-H 2793 2011 ECO-CH-H 1313-1318 1999 MZFC 10652 1999 MZFC 10175-10176 1996 Anolis lemurinus (b) ECO-CH-H 2784-2785 2010 Anolis sagrei ECO-CH-H 2794-2800 2011 Aspidoscelis maslini ECO-CH-H 2792 2011 (a) Misidentified and misspelled first as Hemidactylus tursicus. (b) Neonates with doubtful identification, likely neonates of Anolis sagrei. TABLE 4--Morphological dataa of Aristelliger georgeensis, Anolis allisoni, Anolis sagrei, and Aspidoscelis maslini collected during 2011-2013 from Banco Chinchorro Biosphere Reserve, Quintana Roo, Mexico. Data are presented as Mean [+ or -] 1 SD (range; n). --Indicates no data. Aristelliger georgeensis TL (mm) Females 146.0 [+ or -] 7.1 (141-151; 2) Males 151.6 [+ or -] 20.2 (132-191; 10) SVL (mm) Females 65.0 [+ or -] 4.2 (32-38; 2) Males 71.0 [+ or -] 7.0 (62-84; 11) CL (mm) Females 15.2 [+ or -] 5.0 (11.6-18.7; 2) Males 18.2 [+ or -] 4.2 (11.1-24.2; 11) Mass (g) Females 7.3 [+ or -] 1.1 (6.5-8.1; 2) Males 9.6 [+ or -] 3.3 (5.5-17.0; 10) Anolis allisoni TL (mm) Females 156.0 [+ or -] 18.2 (115-196; 20) Males 198.8 [+ or -] 29.2 (123-261; 51) SVL (mm) Females 57.7 [+ or -] 4.5 (49-65; 21) Males 75.4 [+ or -] 11.7 (45-95; 54) CL (mm) Females 14.6 [+ or -] 2.3 (11.1-20.4; 21) Males 21.1 [+ or -] 4.8 (12.8-30.9; 54) Mass (g) Females 3.5 [+ or -] 0.8 (2.2-4.8; 21) Males 8.6 [+ or -] 3.6 (2.2-19; 53) Anolis sagrei TL (mm) Females 117.9 [+ or -] 31.7 (83-195; 9) Males 150.1 [+ or -] 25.8 (96-228; 50) SVL (mm) Females 48.5 [+ or -] 5.4 (40-59; 11) Males 58.6 [+ or -] 6.6 (41-68; 53) CL (mm) Females 10.7 [+ or -] 1.9 (8-14.7; 11) Males 13.5 [+ or -] 1.7 (9.1-16.6; 53) Mass (g) Females 2.1 [+ or -] 0.5 (1.2-2.8; 11) Males 4.9 [+ or -] 1.7 (1.5-8.8; 52) Aspidoscelis maslini TL (mm) Females 210.8 [+ or -] 32.1 (127-260; 38) Males -- SVL (mm) Females 73.7 [+ or -] 5.6 (62-84; 38) Males -- CL (mm) Females -- Males -- Mass (g) Females 9.2 [+ or -] 2.4 (5-15; 38) Males -- (a) TL: total length; SVL: snout-vent length; CL: cranial length.
|Printer friendly Cite/link Email Feedback|
|Author:||Charruau, Pierre; Perez, Anibal H. Diaz de la Vega; de la Cruz, Fausto R. Mendez|
|Date:||Dec 1, 2015|
|Previous Article:||Reproduction and nutrition of desert mule deer with and without predation.|
|Next Article:||New distributional records for endangered black-capped vireos (Vireo atricapilla) on their wintering grounds in Mexico.|