Herpetology Notes, volume 3: 341-352 (2010) (published online on 12 December 2010) Composition and species richness of herpetofauna in two isolated regions of southern Nicaragua Marco D. Barquero 1 *, Milton Salazar-Saavedra 2, Luis Sandoval 3, Deyling Brenes 4, Fidel Martínez 4 & Alfredo Figueroa 4 Abstract. Basic information about Nicaraguan herpetofauna is still unavailable, although this has begun to change in recent years. Environmental change has been fragmenting pristine habitats, threatening the survival of many species. The aim of this study is to analyze species composition in two isolated regions of Nicaragua. We report a list of amphibians and reptiles occurring at Mancarroncito, an island of the Solentiname Archipelago, and we update information reported for an isolated forest patch of the private reserve El Quebracho. These sites appear to function as refuges for herpetofauna, since they harbour a high diversity in a small area. Keywords. Amphibians, El Quebracho Private Wildlife Reserve, Isolated habitats, Mancarroncito Island, Reptiles, Species composition. Introduction 1 Asociación para la Conservación y el Estudio de la Biodiversidad (ACEBIO); e-mail: marcodba@acebio.org 2 Herpetonicas; e-mail: mescrotalus@yahoo.es 3 Escuela de Biología, Universidad de Costa Rica, Montes de Oca, Costa Rica; e-mail: biosandoval@hotmail.com 4 Fundación para la Conservación y el Desarrollo del Sureste de Nicaragua (Fundación del Río); e-mail: figueroadavi@yahoo.com * corresponding author According to the equilibrium theory of island biogeography, the number of species found in insular habitats is usually lower than the species diversity found in mainland habitats of equal size (MacArthur and Wilson, 1967; Losos and Ricklefs, 2009). However, continued fragmentation of forests has caused a decline in populations inhabiting both mainland and insular environments, creating islands of forest in mainland Figure 1. Map showing localization of the study sites, Mancarroncito Island and El Quebracho.
342 Marco D. Barquero et al. Table 1. List of species of amphibians and reptiles recorded for Mancarroncito Island and El Quebracho Private Wildlife Reserve. Relative abundance of each species according to the site is included (abbreviations are: A = abundant, C = common, U = uncommon). We took into account species that were observed, identified by call (Order Anura) or previously reported for the site. Population trend and distribution for each species countrywide is also included. Taxonomic classification Study site Population Mancarroncito El Quebracho trend Distribution CLASS AMPHIBIA Order Gymnophiona Family Caeciliidae Gymnopis multiplicata -- U Decreasing Caribbean Order Caudata Family Plethodontidae Bolitoglossa striatula -- U Decreasing Caribbean Order Anura Family Bufonidae Chaunus marinus A C Increasing Both slopes Incilius valliceps C A Stable Caribbean Unidentified A 1 -- -- -- Family Centrolenidae Cochranella granulosa -- U 2 Unknown Caribbean Teratohyla pulverata -- U Unknown Caribbean Family Craugastoridae Craugastor bransfordii -- A Decreasing Caribbean Craugastor fitzingeri A A Stable Both slopes Family Dendrobatidae Dendrobates auratus -- C Unknown Caribbean Oophaga pumilio -- C Decreasing Caribbean Family Eleutherodactylidae Diasporus diastema -- A Decreasing Caribbean Family Hylidae Agalychnis callidryas -- C Decreasing Both slopes Dendropsophus ebraccatus -- C 2 Stable Caribbean Dendropsophus microcephalus C -- Increasing Both slopes Hypsiboas rufitelus -- C Stable Caribbean Scinax elaeochrous -- A Stable Caribbean Scinax staufferi C -- Stable Both slopes Trachycephalus venulosus C 2 -- Stable Pacific Family Leptodactylidae Leptodactylus fragilis C U Stable Both slopes Leptodactylus melanonotus U U Stable Both slopes Leptodactylus savagei -- C Stable Caribbean Family Strabomantidae Pristimantis ridens -- C Stable Caribbean Family Ranidae Lithobates warszewitschii -- U Increasing Caribbean areas and threatening survival of many species (Turner, 1996). This fragmentation affects all kinds of organisms, especially those whose distribution is restricted to the forest, require large areas, and have low dispersal capabilities. Amphibians and reptiles are usually lowdispersal organisms with small ranges compared to other vertebrates, such as birds and mammals (Pough et al., 2001; Zug et al., 2001). Therefore, the analysis
Herpetofauna composition and species richness in southern Nicaragua 343 Table 1. continued CLASS REPTILIA Order Testudines Family Emydidae Trachemys scripta C -- Unknown Both slopes Order Crocodylia Family Alligatoridae Caiman crocodilus U 3 -- Unknown Both slopes Order Squamata - Suborder Sauria Family Corytophanidae Basiliscus plumifrons -- U Unclassified Caribbean Basiliscus vittatus U -- Unclassified Both slopes Family Eublepharidae Coleonyx mitratus U -- Unclassified Pacific Family Gekkonidae Gonatodes albogularis A A Unclassified Both slopes Phyllodactylus tuberculosus A -- Unclassified Pacific Sphaerodactylus millepunctatus C U Unclassified Caribbean Family Iguanidae Ctenosaura similis U -- Unclassified Pacific Iguana iguana U 3 -- Unclassified Both slopes Family Polychrotidae Anolis capito -- U Unclassified Caribbean Anolis quaggulus -- C Unclassified Both slopes Anolis limifrons A A Unclassified Caribbean Anolis oxylophus -- U Unclassified Caribbean Family Scincidae Sphenomorphus cherriei U C Unclassified Caribbean Family Teiidae Ameiva festiva -- C Unclassified Caribbean Ameiva undulata C -- Unclassified Both slopes Order Squamata - Suborder Family Boidae Boa constrictor U U 3 Unclassified Both slopes Family Colubridae Chironius sp. -- U -- -- Family Dipsadidae Imantodes cenchoa -- U Unclassified Caribbean Rhadinaea decorata -- U Unclassified Caribbean Sibon nebulatus U U Unclassified Caribbean Urotheca decipiens -- U Unclassified Caribbean Family Viperidae Bothrops asper -- U 3 Unclassified Caribbean Porthidium nasutum -- U Stable Caribbean 1 Juveniles too small to make an appropriate in situ identification. 2 Species identified by its call, but not observed during samplings. 3 Species reported previously for the site, but not observed during samplings. of the herpetofauna composition and routes taken by organisms to colonize different environments has been of great scientific interest (Savage, 1983, 2002). Historically, the Nicaraguan herpetofauna has received little attention from the scientific community, which explains the significantly lower number of species reported for Nicaragua compared to neighboring countries (Brattstrom and Howell, 1954; Campbell and
344 Figure 2. Number of species of amphibians and reptiles found at Mancarroncito Island (A) and El Quebracho (B) classified according to their main distribution in Nicaragua. Howell, 1965; Villa, 1971). However, in recent years the number of species recorded has risen steadily due to an increasing number of researchers interested in the study Marco D. Barquero et al. of amphibians and reptiles in the country. Currently, 71 species of amphibians and 177 reptiles are recognized for Nicaragua (Köhler, 2001; Ruiz and Buitrago, 2003), although the species list is not a definite one and a greater sampling effort is still required for many regions. Although Nicaragua has a wide diversity of ecosystems that may harbour a great diversity of species (MARENA, 2001; Meyrat, 2001; Rueda, 2007), many ecosystems remain unexplored. At the same time, most areas are facing sustained loss of habitat and degradation through forest fragmentation, increase of the agricultural frontier, and pollution (Mendoza et al., 2001; UNEP, 2003; Rueda, 2007). Although ecosystems from the Pacific slope exhibit severe deterioration, those from the Caribbean slope remain relatively unaltered even when sampling of this area remains scarce (Rueda, 2007). We visited two poorly explored sites from southern Nicaragua that are facing anthropogenic pressures. El Quebracho Private Wildlife Reserve protects an isolated rainforest patch, while at Mancarroncito Island there is a transitional wet-dry tropical forest. Forest fragmentation has occurred at both sites, so that these reserves could potentially serve as refuges for several organisms. This is of great importance especially for amphibians and reptiles, which are facing population declines worldwide (Gibbons et al., 2000; Young et al., 2001). Therefore, the aim of this paper is to analyze the herpetofauna species composition found at El Quebracho Private Wildlife Reserve and Mancarroncito Island, in order to generate information on the status of Nicaraguan herpetofauna populations in isolated areas. Materials and Methods Figure 3. Percentage of amphibian (A) and reptile (B) species classified as abundant, common and uncommon at Mancarroncito Island and El Quebracho Private Wildlife Reserve. Study sites The study was conducted at two sites. The first locality, Mancarroncito Island (11º10 53 N, 85º03 23 W, 40 m asl), has an extension of 190 ha and belongs to Solentiname Archipelago National Monument, located in Lake Nicaragua, Río San Juan Department (Fig. 1). The habitat is disturbed, transitional wet-dry tropical forest, with an annual average precipitation of 1500 mm and annual average temperature of 26-28 ºC. The second site, El Quebracho Private Wildlife Reserve (11º09 58 N, 84º24 21 W, 60 m asl), covers an area of 86 ha and is located in the Río San Juan Department, El Castillo Municipality, at the buffer zone of Indio Maíz Biological Reserve (Fig. 1). The habitat is tropical wet forest, with an annual average temperature of 24-26 ºC and an annual average precipitation of 3000 mm. Information on the herpetofauna for both sites is limited at best. For Mancarroncito Island there are no reliable records on the number of species of amphibians and reptiles, while 5 species of amphibians and 19 reptiles have been previously reported for El Quebracho (MA- RENA, 2001).
Herpetofauna composition and species richness in southern Nicaragua 345 in Nicaragua (IUCN, 2010), and (2) we examined its distribution in the country and classified each organism as belonging to Caribbean slope, Pacific slope or both slopes (Köhler, 2001; Ruiz and Buitrago, 2003). For the latter classification we used only doubtless records recognized for each species (HerpNET, 2010). Finally, we created a photographic record of each species captured at both study sites. Figure 4. Number of species of amphibians and reptiles, classified by IUCN (2010) threatened categories (A) and national population trend (B). Codes for categories of threat are: LC = Least Concern, LR / NT = Lower Risk / Near Threatened, NC = Not Classified. Methodology The study was carried out during the first two weeks of September 2009, with one-week sampling for each site. We first visited Mancarroncito Island, followed by El Quebracho Private Wildlife Reserve. We walked along the trails of each site to collect data during diurnal (6 am - 4 pm) and nocturnal (7 pm - 11 pm) samplings. We sampled most of the habitats present at each site (forest, pastures, plantations, streams), exploring a different area every day to avoid pseudoreplication. We used visual encounter survey techniques as described by Crump and Scott (1994) to find amphibians and reptiles on the ground and vegetation. For each individual captured the following data were recorded: study site, species, sex, and age (adult or juvenile). In addition, frogs we were unable to visually distinguish were identified by calls. We also included species previously reported for each site. For most of the species, we use the taxonomic classification suggested by Savage & Bolaños (2009); however, we disagree with these authors about the use of Norops and Scinax elaeochroa and accept the use of Anolis suggested by Poe (2004) and S. elaeochrous suggested by Köhler & Böhme (1996). We used the species list obtained to compare the degree of similarity among the herpetofaunal communities of each study site by using the Jaccard index. Since none of the individuals captured were marked, we could not establish absolute abundance of each species. Therefore, we categorized relative abundance as Abundant (> 10 individuals observed or heard), Common (6-10 individuals) and Uncommon (less than 6 individuals). Also, for each species: (1) information was obtained on the conservation status (i.e. the likelihood of one species to remain extant in the near future) and population trend Results We identified a total of 23 amphibian species distributed in 11 families and 25 reptile species distributed in 13 families. For Mancarroncito Island we found 22 species (8 amphibians and 14 reptiles), whereas 36 species (20 amphibians and 16 reptiles) were recorded for El Quebracho (Table 1). All these species were captured and photographed, with the exception of 3 species from Mancarroncito (one frog identified by its call and two reptiles reported previously for the site) and 5 from El Quebracho (two frogs identified by their call, two reptiles reported previously for the site, and one snake that escaped). The degree of similarity between both sites was low (Jaccard index = 0.22). It was determined that species identified on Mancarroncito Island, both amphibians and reptiles, had a wide distribution in Nicaragua, most of them extending across both slopes (Fig. 2A). By contrast, most species from El Quebracho had a distribution restricted to the Caribbean slope (Fig. 2B). At both sites, most amphibian species (> 65%) were abundant or common (Fig. 3A). Only Leptodactylus melanonotus was uncommon at Mancarroncito Island, while at El Quebracho seven species were uncommon (Table 1). None of the amphibian species recorded at either site are classified as threatened (Fig. 4A), although six species appear to have declining populations in the country (Fig. 4B). In the case of reptiles, most species (> 55%) were uncommon at both sites (Fig. 3B). Six species at Mancarroncito Island and five at El Quebracho were abundant or common (Table 1). Of all the species identified, only one is classified in a category of threat, while most species were not ranked in any category (Fig. 4). Discussion Although more than 40% of Nicaragua is still covered by forest (Rueda, 2007), little is known about biodiversity present in this country. In recent decades, renewed scientific attention has resulted in the creation of a species list as complete as possible, taking into account sites that had not been previously visited or for which there was little information.
346 Marco D. Barquero et al. Figure 5. Amphibians found both at Mancarroncito Island (MI) and El Quebracho Private Wildlife Reserve (EQ), Nicaragua. No photos available for species identified by its call. A. Gymnopis multiplicata (EQ), B. Bolitoglossa striatula (EQ), C. Chaunus marinus (MI), D. Incilius valliceps (EQ), E. Teratohyla pulverata (EQ), and F. Craugastor bransfordii (EQ). Here we present new data on amphibians and reptiles inhabiting one island from Solentiname Archipelago, as well as updated information for a private wildlife reserve of the western portion of the Rio San Juan Department. Our findings complement the available information for southern Nicaragua and highlight that our study sites may function as islands, making them of great scientific and conservation interest. Although data obtained during this study are not complete, we can already identify some clear patterns. Species composition differed between both sites. In Mancarroncito Island we found a mixture of species from both the Caribbean and Pacific slopes. The presence of species from both slopes mainly originates from two factors: (1) Mancarroncito is located only 11 km from the nearest mainland site, and (2) there are no significant geographical barriers to regulate migration of individuals between dry and wet forest habitats in Southern Nicaragua. We also found that amphibian populations inhabiting the island are abundant and most of these species are not threatened and have stable populations countrywide. This indicates that populations from Mancarroncito face no imminent extinction risk. In the case of
Herpetofauna composition and species richness in southern Nicaragua 347 Figure 6. G. Craugastor fitzingeri (MI), H. Dendrobates auratus (EQ), I. Oophaga pumilio (EQ), J. Diasporus diastema (EQ), K. Agalychnis callidyas (amplexus from EQ), and L. Dendropsophus microcephalus (MI). reptiles, some species of lizards (eg. Gekkonids and Anoles) occur in high numbers at this site, but it was not possible to determine the conservation status of most populations as they were uncommon. Longterm population studies are needed to determine the fluctuations of these species at Mancarroncito. The origin of the herpetofauna from El Quebracho is mostly Caribbean. Proximity to this area and climatic conditions on the site (high humidity and high precipitation) facilitate colonization of Caribbean species and make arrival of Pacific ones unlikely. The hereby reported list of 36 species of amphibians and reptiles found at El Quebracho, although higher than the previous one reported for the site (MARENA, 2001), is not a definitive one. Sunyer et al. (2009) found 35 species of amphibians in three sites near El Quebracho (Bartola, Río Sarnoso, and Dos Bocas de Bartola-El Almendro), whereas in the present study we only observed 20 species. With regard to the conservation status of the species at these sites, we cannot obtain a clear conclusion from our data. Nevertheless, a higher proportion of species were uncommon at El Quebracho compared to Mancarroncito Island, so there could be greater pressure on these populations. Despite being separated by only 70 km, the two sites
348 Marco D. Barquero et al. Figure 7. M. Hypsiboas rufitelus (EQ), N. Scinax elaeochrous (juvenile from EQ), O. Scinax staufferi (MI), P. Leptodactylus fragilis (MI), Q. Leptodactylus melanonotus (EQ), R. Leptodactylus savagei (subadult from EQ), S. Pristimantis ridens (EQ), and T. Lithobates warszewitschii (EQ).
Herpetofauna composition and species richness in southern Nicaragua 349 Figure 8. Reptiles found both at Mancarroncito Island (MI) and El Quebracho Private Wildlife Reserve (EQ), Nicaragua. No photos available for species reported previously for the study sites, Chironius sp. and Urotheca decipiens. A. Trachemys scripta (MI), B. Basiliscus plumifrons (EQ), C. Basiliscus vittatus (MI), D. Coleonyx mitratus (MI), E. Gonatodes albogularis (MI), and F. Phyllodactylus tuberculosus (MI). visited differed in species composition and species richness. However, both sites seem to function as refuges, since they harbour a high diversity of species in a small area. Mancarroncito Island contains the most preserved forest in the Solentiname Archipelago, while El Quebracho is surrounded by farms and ranches. Therefore, conservation of these sites is of great importance, so they can be reservoirs of genetic material. Furthermore, the species accumulation curve for both sites has not reached yet an asymptote and more species are expected to appear with increasing sampling effort. This is the trend for the entire territory of Nicaragua, as new records have been reported steadily during the last decade. Remarkably, during this study we found a colubrid snake (Urotheca decipiens) at El Quebracho that is a new record for Nicaragua (Salazar-Saavedra et al., in preparation), which is encouraging to keep exploring the country. Acknowledgments. We are very grateful with people in charge of Fundación para la Conservación y el Desarrollo del Sureste de Nicaragua (Fundación del Río), especially with Antonio Ruiz Meléndez for his support to visit the study sites. We also thank Robert Puschendorf and Dani Chandrasoma for their comments to improve the manuscript.
350 Marco D. Barquero et al. Figure 9. G. Sphaerodactylus millepunctatus (MI), H. Ctenosaura similis (MI), I. Anolis capito (EQ), J. Anolis limifrons (MI), K. Anolis oxylophus (EQ), and L. Anolis quaggulus (EQ). References Brattstrom, B.H., Howell, T.R. (1954): Notes on some collections of reptiles and amphibians from Nicaragua. Herpetologica 10: 114-123. Campbell, H.W., Howell, T.R. (1965): Herpetological records from Nicaragua. Herpetologica 21: 130-140. Crump, M.A., Scott Jr., N.J. (1994): Visual encounter surveys. In: Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians, p. 84-92. Heyer, W.R., Donnelly, M.A., McDiarmid, R.W., Hayek, L.C., Foster, M.S., Eds., Washington, Smithsonian Institution Press. Gibbons, J.W., Scott, D.E., Ryan, T.J., Buhlmann, K.A., Tuberville, T.D., Metts, B.S., Greene, J.L., Mills, T., Leiden, Y., Poppy, S., Winne, C.T. (2000): The global decline of reptiles, déjà vu amphibians. BioScience 50: 653-666. HerpNET. (2010): HerpNET data portal. http://www.herpnet. org. Last accessed 5 February 2010. IUCN. (2010): IUCN Red List of Threatened Species. Version 2010.1. http://www.iucnredlist.org. Last accessed 5 February 2010. Köhler, G. (2001): Anfibios y Reptiles de Nicaragua. Offenbach, Herpeton. Köhler, J., Böhme, W. (1996): Anuran amphibians from the region of Pre-Cambrian rock outcrops (inselbergs) in northeastern Bolivia, with a note on the gender of Scinax Wagler, 1830 (Hylidae). Rev. Fr. Aquariol., Herpetol. 23: 133-140.
Herpetofauna composition and species richness in southern Nicaragua 351 Figure 10. M. Sphenomorphus cherriei (EQ), N. Ameiva festiva (subadult from EQ), O. Ameiva undulata (MI), P. Boa constrictor (MI), Q. Imantodes cenchoa (EQ), R. Rhadinaea decorata (EQ), S. Sibon nebulatus (MI), and T. Porthidium nasutum (EQ).
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