LAGUNA DEL TIGRE 2013-2014 The Herpetofauna of Estación Biológica las Guacamayas and Surrounding Areas Laguna del Tigre National Park, Guatemala Author: Rowland Griffin. Translation: Aitor Cevidanes. License: : 038/2013
2013-2014 The Herpetofauna of Estación Biológica las Guacamayas & Surrounding Areas Laguna del Tigre National Park Guatemala (CONAP) Author: Rowland Griffin Translation: Aitor Cevidanes 04 September 2014 Indigo Expeditions info@explorewithindigo.com 0 2
Foreward Acknowledgements Indigo Expeditions would like to thank the staff of the regional office of the Consejo Nacional de Areas Protegidas (CONAP) for their continued support to our research. We also thank Jeovany Tut Rodriguez, Cornelio Chable and the staff at Estación Biológica Las Guacamayas for their support and enthusiasm. Finally we thank our volunteers for their commitment in the field and without whom this research would not have been possible. With thanks Rowland Griffin Director of Research Co-Founder of Indigo Expeditions This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License. 0 3
Introduction The Herpetofauna of Estación Biológica las Guacamayas During our fieldwork in 2013 and 2014 we continued to investigate the effects of agriculture on the reptile and amphibian assemblage in the forest around Estación Biológica las Guacamayas (Las Guacamayas) and the surrounding areas in the southeastern area of Laguna del Tigre National Park. Las Guacamayas has a varied landscape within and bordering its reserve land. Las Guacamayas is situated at the southern border of the Laguna del Tigre National Park (LTNP), the border of which is delineated by the Rio San Pedro. The LTNP side of the river is characterised by the presence of limestone outcrops that rise relatively sharply from the river bed, the vegetation here is Tropical Dry Forest. The southern side of the river is a flat landscape of seasonally inundated grass/swamps and thorn scrub that borders the Rio San Pedro and Rio Sacluc. To the East the Tropical Dry Forest in bordered by agriculture of the local community, known as Paso Caballos. 0 4
Methodology Four forest categories (bosque alto, bosque bajo, natural edge, and agricultural edge) were sampled at Las Guacamayas using Visual Encounter Surveys (VES) (Heyer et al. 1994; McDiarmid et al. 2012). Surveys were conducted during two field work periods, the first from 4th November to 30th December 2013 and the second from 17th to 30th June 2014. Visual Encounter Surveys (VES) Transects were walked at a suitably slow enough pace to allow thorough examination of the vegetation for reptiles and amphibians. The vegetation surrounding each transect was surveyed up to one metre either side of the transect and up to two metres in height. Each transect was surveyed at least once during the day and twice during the night. At the start of each transect the following environmental data was recorded: time of start(24hr), air temperature (ºC), relative humidity (%), and cloud cover (%). Additionally, time of finish of each transect (24hr), daily rainfall (mm), daily barometric pressure (hpa) and daily moon phase were recorded. When safe to do so, each individual encountered was captured and the following data recorded: time encountered (24hr), location was recorded using a Garmin GPSmap 62s, activity (rest, basking, foraging), position (leaf litter, shrub layer, branch [if on a branch the diameter of the perch was measured in cm], and height from ground [cm]) each individual was first observed body temperature before capture (if possible and calculated with an infrared thermometer in ºC), species, age (adult, juvenile, neonate), sex (if possible), length (mm) and weight (g). Biometric data for amphibians and most lizards was taken in the field. All snakes captured were brought back to Las Guacamayas for collection of biometric data for ease and were marked for identification using cautery branding of the ventral scales following an adapted method described by Winne et al. (2006), see Appendix 1 for details of the marking scheme. All individuals were released at the point of capture within 48 hours. Additional Targeted Habitat Surveys Additional surveys of trails and other interesting habitats surrounding Las Guacamayas (for example, the swamp and thorn scrub near to Rio Sacluc) were conducted on an ad-hoc basis. Data collected was the same as for VES. 0 5
Data Analysis Species accumulation curves, Mau Tau with 95% confidence intervals, were constructed to describe the diversity of amphibian and reptile fauna at Las Guacamayas. Species richness estimators were calculated to evaluate the effectiveness of the survey methods used in relation to the target habitat types, using both - nonparametric incidence-based estimators (Bootstrap, Chao 2, ICE, Jacknife 1 and 2) and - abundance-based data (ACE and Chao 1). Species accumulation analysis was performed using EstimateS 7.5 software (Colwell 2005). Species diversity was compared between the target habitat types using Friedman s Two-Way ANOVA. Analysis of species diversity was performed using Minitab 15.1.0.0. 0 6
Results Including casual observations, a total of 65 species of reptile and amphibian were recorded during the periods 4th November to 30th December 2013 and 17th to 30th June 2014. Of these 49 were reptiles (of which one was a crocodilian, 5 were turtles, 18 were lizards and 25 were snakes), and 16 were amphibians (of which one was a salamander and 15 were anurans). For a full species list see Appendix 2. Species Accumulation Species accumulation curves (Mao Tao) forall four habitat types were carried out using data collected from this study and our previous study in May and June 2013. They did not reach stability (Fig. 1). The species richness estimators consistently produced greater results than the actual numbers of species encountered during this project (Table 1). Estimators Agricultural Bosque Bosque Bajo Natural Edge Alto Edge ACE 54.98 42.95 36.22 36.35 ICE 45.06 46.43 38.05 35.95 Chao 1 54.5 46 36.09 35.33 Chao 2 64 40.25 36 35.06 Jacknife 1 22.75 40.73 39.6 38.53 Jacknife 2 29.61 46.29 39.98 39.82 Bootstrap 17.54 33.83 36.08 34.45 Observed 14 29 33 31 Table 1: Species richness estimators of the reptile and amphibian assemblage at Las Guacamayas. 0 7
Results a) b) c) d) Fig 1: Species accumulation curves (Mao Tao) for a) agricultural edge, b) bosque alto, c) bosque bajo and d) natural edge at Las Guacamayas. Time represented as number s on the x-axis and number of predicted species is on the y-axis. 0!8
Results Species Diversity Analysis We conducted Friedman s Two-Way ANOVAs on VES data from the data collection periods of the current study only (i.e. 4th November to 30th December 2013 and 17th to 30th June 2014). The number of species recorded during the VES surveys are described in Table 2. There was a significant difference in diversity between species assemblage across different habitat types at Las Guacamayas (F=23.08, P=0.000, Agricultural Bosque Bosque Natural All Edge Alto Bajo Edge Habitats Number of 13 24 31 26 42 Table 2: Comparison of observed numbers of species by habitat type. df=3) (Table 2). We found significant differences in assemblage diversity between Agricultural Edge and Bosque Bajo, and Natural Edge, between Bosque Alto and Bosque Bajo, and F P value df Agricultural Edge vs Bosque Alto 2.88 0.09 1 Agricultural Edge vs Bosque Bajo 17.36 0 1 Agricultural Edge vs Natural Edge 4.02 0.045 1 Bosque Alto vs Bosque Bajo 8.6 0.003 1 Bosque Alto vs Natural Edge 1.17 0.28 1 Bosque Bajo vs Natural Edge 4.67 0.031 1 All habitat 23.08 0 3 Table 3: Comparison of diversity of herpetofauna species assemblage at Las Guacamayas as determined by two-way ANOVA s. Statistically significant differences are highlighted in bold. 0 9
Discussion During this study we recorded 65 species of amphibians and reptiles in the forests surrounding Las Guacamayas. Of which, seven of these were new records for Laguna del Tigre National Park, they include the frogs Gastrophryne elegans and Eleutherodactylus leprus, the lizards Sphaerodactylus millepunctatus and Norops sericeus, and the snakes Adelphicos quadrivirgatus, Ninia diademata and Scaphiodontophis annulatus (Lee 1996). This increases the total number of amphibians and reptiles recorded in Laguna del Tigre National Park to 81 species and corroborates the findings of our initial study in 2013 that many more species remain to be found in the park (Project Chicchan 2013). We believe that this shows that Laguna del Tigre National Park is a key habitat for the amphibian and reptile species of Northern Petén and the Yucatán Peninsular. Additionally, our accumulation curves (Fig. 1) show that further study of the herpetofauna of the National Park will increase this number further. This study found that the reptile and amphibian species assemblage diversity was significantly lower in habitat that was associated with agricultural areas to the east of Las Guacamayas when compared to Bosque Bajo and Natural Edge but not when compared to Bosque Alto. Additionally, there was no significant difference in species assemblage diversity between Natural Edge and Bosque Alto. We believe the lack of difference in diversity between Bosque Alto and Agricultural Edge, and between Bosque Alto and Natural Edge is due to both the Agricultural Edge and Natural Edge habitats we surveyed being part of the Alto habitat. In the future we recommend surveying areas of agricultural edge that are at the edge of Bosque Bajo habitat to see if this pattern is still observed there. The effects of fragmentation on the ecology of forests and the species that are found in them have been well documented (Lehtinen et al 2003; McGarigal & Cushman 2002; MacNally & Brown 2001; Villard et al 1999). Our work at Estación Biológica las Guacamayas continues to show that Laguna del Tigre National Park is an important area for reptile and amphibian diversity in Northern Guatemala, additionally this study shows that the reptile and amphibian assemblage of the area is less diverse in areas close to agricultural activity. This study supports the need for the maintenance of the national park and its flora and fauna to continue to conserve the biodiversity of the Maya Biosphere Reserve. 0 10
References Colwell, R.K. 2005. EstimateS 7.5: Statistical estimation of species richness and shared species from samples. Department of Ecology and Evolutionary Biology, University of Connecticut, Connecticut. Heyer, W.R., M.A. Donnelly, R.W. McDiarmid, L-A.C. Hayek, & M.S. Foster. 1994. Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. Smithsonian Institution Press. Washington. Lee, J.C. 1996. The Amphibians and Reptiles of the Yucatán Peninsular. Comstock, Michigan. Lehtinen, R.M., J.-B. Ramanamanjato, & J.G. Raveloarison. 2003. Edge Effects and Extinction Proneness in a Herpetofauna from Madagascar. Biodiversity and Conservation. 12. Pp. 1357-1370. McDiarmid, R.W., M.S. Foster, C. Guyer, J.W. Gibbons, & N. Chernoff. 2012. Reptile Biodiversity: Standard Methods for Inventory and Monitoring. University of California Press. Berkeley. McGarigal, K. & S.A. Cushman. 2002. Comparative Evaluation of Experimental approaches to the Study of Fragmentation Effects. Ecological Applications. 12:2. Pp. 335-345. MacNally, R. & G.W. Brown. 2001. Reptiles and Habitat Fragmentation in the Box- Ironbark Forests of Central Victoria, Australia: Predicitons, Compositional change and Faunal Nestedness. Oecologia. 128. Pp. 116-125. Villard, M.-C., M.K. Trzcinski, & G. Merriam. 1999. Fragmentation Effects on Forest Birds: Relative Influence of Woodland Cover and Configuration on Landscape Occupancy. Conservation Biology. 13:4. Pp 774-783. Winne, C.T., J.D. Willson, K.M. Andrews, & R.N. Reed. 2006. Efficacy of Marking Snakes with Disposable Medical Cautery Units. Herpetological Review. 37:1. Pp 52-54. 0 11
Appendix I Diagram for marking snakes using electrocautery ophthalmic medical pens. In this example the individual has been marked with the ID number 36 ( from Winne et al. 2006). 0 12
Appendix II List of species recorded at Las Guacamayas. Where changes in nomenclature have recently occurred the previous scientific name is included in parentheses. ** denotes an introduced non-native species. FAMILY May/June 2013 2013/14 CI RAP OTHER Species PLETHODONTIDAE Bestelmeyer & Alonso (2000). anecdotal observations verified by the author 1 Bolitoglossa mexicana X X BUFONIDAE 2 Chaunus (Bufo) marinus X X X X 3 Incilius (Bufo) valliceps X X X X MICROHYLIDAE 4 Hypopachus variolosus X X X 5 Gastrophryne elegans X HYLIDAE 6 Agalychnis callidryas X X X X 7 Dendrosophus (Hyla) microcephala X X* X 8 Tlalocohyla (Hyla) loquax X X 9 Tlalocohyla (Hyla) picta X 10 Trachycephalus (Phrynohyas) venulosus X X X X 11 Triprion petasatus X X 12 Scinax staufferi X X 13 Smilisca baudini X X X X ELEUTHERODACTYLIDAE 14 Eleutherodactylus leprus X* 13
Appendix II FAMILY May/June 2013 2013/14 CI RAP OTHER Species LEIUPERIDAE Bestelmeyer & Alonso (2000). anecdotal observations verified by the author 15 Engystomops (Physalaemus) pustulosus X X X LEPTODACTYLIDAE 16 Leptodactylus fragilis (labialis) X X X X 17 Leptodactylus melanolotus X* X X X RANIDAE 18 Rana (Lithobates) brownorum (berlandieri) X X X X 19 Rana (Lithobates) vaillanti X X X GEKKONIDAE 20 Coleonyx elegans X X X X 21 Hemidactylus frenatus** X* X* X 22 Sphaerodactylus glaucus X* X* X 23 Sphaerodactylus millepunctatus X* 24 Thecadactylus rapicauda X* X* X TEIIDAE 25 Ameiva festiva X X X 26 Ameiva undulata X* X X IGUANIDAE 27 Basiliscus vittatus X X X X 28 Corytophanes cristatus X X 29 Corytophanes hernandesi X X 30 Iguana iguana X* X* X 14
Appendix II FAMILY May/June 2013 2013/14 CI RAP OTHER Species Bestelmeyer & Alonso (2000). anecdotal observations verified by the author 31 Norops capito X X X 32 Norops lemurinus (bourgeaei) X X X X 33 Norops pentaprion X 34 Norops sagrei X 35 Norops sericeus X* 36 Norops tropidonotus X 37 Norops uniformis X X X 38 Sceloporus teapensis (variabilis) X* X* X SCINCIDAE 39 Eumeces sumicrasti X* 40 Mesoscincus schwartzi X* X* 41 Mabuya unimarginata (brachiopoda) X* X* X 42 Sphenomorphus cherriei X X BOIDAE 43 Boa constrictor X* X X COLUBRIDAE 44 Adelphicos quadrivirgata X 45 Clelia scytalina X* X* 46 Coniophanes bipunctatus X* X 47 Coniophanes imperialis X X X 48 Coniophanes schmidti (quinquevittatus) X X X 49 Drymobius margaritiferus X X X 15
Appendix II FAMILY May/June 2013 2013/14 CI RAP OTHER Species Bestelmeyer & Alonso (2000). anecdotal observations verified by the author 50 Ficimia publia X* X 52 Imantodes cenchoa X X X X 53 Lampropeltis triangulum X* X 54 Leptodeira frenata X 55 Leptodeira septentrionalis (polysticta) X X X 56 Leptophis ahaetula X 57 Leptophis mexicana X X* 58 Mastigodryas (Dryadophis) melanolotus X* X COLUBRIDAE 59 Ninia diademata X 60 Ninia sebae X X X 61 Oxybelis aneus X* X 62 Oxybelis fulgidus X* X 63 Oxyrhopus petola X X 64 Scaphiodontophis annulatus X* 65 Senticolis triaspis X 66 Sibon nebulata X X 67 Spilotes pullatus X 68 Tantillita canula X* 69 Tretanorhinus nigroluteus X X* X 70 Tropidodipsas (Sibon) fasciatus X* 16
Appendix II FAMILY May/June 2013 2013/14 CI RAP OTHER Species 71 Tropidodipsas (Sibon) sartori X X Bestelmeyer & Alonso (2000). anecdotal observations verified by the author 72 Xenodon rabdocephalus X* X X ELAPIDAE 73 Micrurus diastema X* X X VIPERIDAE 74 Bothrops asper X X X KINOSTERNIDAE 75 Kinosternon leucostomum X X X 76 Kinosternon acutum X X 77 Staurotypus triporcatus X DERMATEMYDIDAE 78 Dermatemys mawi X X EMYDIDAE 79 Trachemys scripta X* X* X X 80 Rhinoclemys areolata X X CROCODYLIA 81 Crocodylus moreleti X* X X X 17
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