Abstract
Six species of giant alpha anoles of the genus Dactyloa are known to occur in western Panama: Dactyloa casildae, D. frenata, D. ibanezi, D. insignis, D. kunayalae, and D. microtus. Based on own material collected along the highlands in Bocas del Toro, Chiriquí, and Veraguas provinces and the Comarca Ngöbe-Buglé of western Panama, we review their vari-ation in morphological characters and the 16S rRNA mitochondrial gene. Our results support all six nominal taxa, but re-veal considerable genetic differentiation between populations of the two highland species, D. casildae and D. microtus, respectively, from different localities. Correlated morphological differences confirm the existence of a cryptic species among populations currently assigned to D. microtus, which we describe as Dactyloa ginaelisae sp. nov. We provide point distribution maps, morphology and color descriptions, photographs in life, conservation status assessments, and an iden-tification key for all seven species.References
ANAM (2004) Diagnóstico biológico y sociocultural del Humedal de Importancia Internacional San San Pond Sak. Anexo al Plan de manejo del Humedal de Importancia Intermacional San San Pond Sak. Autoridad Nacional del Ambiente (ANAM), Panamá.
Arosemena, F.A., Ibáñez D., R. & de Sousa, F. (1992 “1991”) Una especie nueva de Anolis (Squamata: Iguanidae) del grupo latifrons de Fortuna, Panamá. Revista de Biologia Tropical, 39, 255–262.
Auth, D.L. (1994) Checklist and bibliography of the amphibians and reptiles of Panama. Smithsonian Herpetological Information Service, 98, 1–59.
Barbour, T. (1923) Notes on reptiles and amphibians from Panama. Occasional Papers of the Museum of Zoology, University of Michigan, 129, 1–16.
Berthold, A.A. (1845) Über verschiedene neue oder seltene Reptilien aus Neu-Granada und Crustaceen aus China. Abhandlungen der Königlichen Gesellschaft der Wissenschaften in Göttingen, 3, 3–32.
Boulenger, G.A. (1898) An account of the reptiles and batrachians collected by Mr. W. F. H. Rosenberg in western Ecuador. Proceedings of the Zoological Society of London, 1898, 107–126.
Boulenger, G.A. (1885) Catalogue of the lizards in the British Museum (Natural History). Vol. 2, Second edition, London, xiii+497 pp.
Breder, C.M. (1946) Amphibians and reptiles of the Rio Chucunaque drainage, Darién, Panama, with notes on their life histories and habits. Bulletin of the American Museum of Natural History, 86, 379–435.
Carrizo, A.R. (2010) Riqueza y abundancia de la herpetofauna de la cuenca alta del Río Santa María, Santa Fe, Veraguas. Master thesis. Universidad Autónoma de Chiriquí, Davíd. Available from http://www.senckenberg.de/files/content/forschung/abteilung/terrzool/herpetologie/herpetofauna_cuenca_alta_rio_santa_maria_veraguas_panama_carrizo_2010.pdf
(accessed 26 June 2011).Castañeda, M.d.R. & de Queiroz, K. (2011) Phylogenetic relationships of the Dactyloa clade of Anolis lizards based on nuclear and mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution, 61, 784–800.
http://dx.doi.org/10.1016/j.ympev.2011.07.004Chun, W. (2010) Miscellaneous notes on some rare and unusual anoles. In: Mahler, D.L.; Herrel, A.; Losos, J.B. (Eds.), Anolis Newsletter VI. Museum of Comparative Zoology at Harvard University, Cambridge, USA, pp. 14–22.
Clement, M., Posada, D. & Crandall, K. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology Notes, 9, 1657–1660.
http://dx.doi.org/10.1046/j.1365-294x.2000.01020.xCope, E.D. (1871) Ninth contribution to the herpetology of tropical America. Proceedings of the Academy of Natural Sciences of Philadelphia, 23, 200–224.
Cope, E.D. (1876 "1875") On the Batrachia and Reptilia of Costa Rica. Journal of the Academy of Natural Sciences of Philadelphia, ser. 2, 8, 93–154.
Cope, E.D. (1899) Contributions to the herpetology of New Granada and Argentina, with descriptions of new forms. The Philadelphia Museum Science Bulletin, 1, 11–22.
de Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56, 6, 879–886.
http://dx.doi.org/10.1080/10635150701701083de Sousa, F. (1999) Fortuna, reserva biológica. Evaluación del posible impacto ecológico sobre la fauna existente en el área del nuevo embalse del proyecto hidroeléctrico La Fortuna. Editorial Universitaria "Carlos Manuel Gasteazoro", Panamá, 207 pp.
Drummond, A.J., Ashton, B., Cheung, M., Heled, J., Kearse, M., Moir, R., Stones-Havas, S., Thierer, T. & Wilson, A. (2010) Geneious v.4.8.5. Available from: www.geneious.com (accessed 10 November 2011).
Dunn, E.R. (1937) The giant mainland anoles. Proceedings of the New England Zoological Club, 15, 5–9.
Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 1–19.
http://dx.doi.org/10.1186/1471-2105-5-113Etheridge, R. (1959) The relationships of the anoles (Reptilia: Sauria: Iguanidae). An interpretation based on skeletal morphology. Ph.D. Dissertation, University of Michigan, Ann Arbor, Michigan, USA.
Fläschendräger, A. & Wijffels, L.C.M. (2009) Anolis. Im Biotop und Terrarium. Natur und Tier-Verlag, Münster, 319 pp.
Frank, N. & Ramus, E. (1995) A complete guide to scientific and common names of reptiles and amphibians of the world. NG Publishing, Pottsville, 377 pp.
Guyer, C. & Savage, J.M. (1986) Cladistic relationships among anoles (Sauria: Iguanidae). Systematic Zoology, 35, 509–531. http://dx.doi.org/10.2307/2413112
Hamad, N. (2009) Diversität, Taxonomie und Zoogeographie der Herpetofauna eines Untersuchungsgebietes in der Reserva Forestal Fortuna (Chiriquí, Panama). Diploma thesis. Goethe-Universität, Frankfurt am Main, 126 pp.
Hart, M.W. & Sunday, J. (2007) Things fall apart: biological species form unconnected parsimony networks. Biology Letters, 3, 509–512. http://dx.doi.org/10.1098/rsbl.2007.0307
Hertz, A., Lotzkat, S., Carrizo Diaz, A.R., Ponce, M., Köhler, G. & Streit, B. (2012) Field notes on findings of threatened amphibian species in the central mountain range of western Panama. Amphibian and Reptile Conservation, 6, 9–30.
Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965–1978. http://dx.doi.org/10.1002/joc.1276
Hofer, U. & Bersier, L.-F. (2001) Herpetofaunal diversity and abundance in tropical upland forests of Cameroon and Panama. Biotropica, 33, 142–152.
http://dx.doi.org/10.1646/0006-3606(2001)033[0142:HDAAIT]2.0.CO;2Holdridge, L.R. (1967) Life zone ecology. Tropical Science Center, San Jose, Costa Rica, 206 pp.
Holdridge, L.R. (1971) Forest environments in tropical life zones. A pilot study. Pergamon Press, Oxford, New York, xxxi+747 p.
Huelsenbeck, J.P. & Ronquist, F. (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755. http://dx.doi.org/10.1093/bioinformatics/17.8.754
Hulebak, E., Poe, S., Ibáñez D., R. & Williams, E.E. (2007) A striking new species of Anolis lizard (Squamata, Iguania) from Panama. Phyllomedusa, 6, 5–10.
Ibáñez D., R., Arosemena, F.A., Solís, F.A. & Jaramillo A., C.A. (1995 "1994") Anfibios y reptiles de la Serranía Piedras-Pacora, Parque Nacional Chagres. Scientia (Panamá), 9, 17–31.
Ibáñez D., R., Jaramillo A., C.A., Arrunátegui, M., Fuenmayor, Q. & Solís, F.A. (1997 "1995") Inventario biológico del Canal de Panamá. Estudio herpetológico. In: Tejera, V.H.; Ibáñez D., R.; Arosemena G., G. (Eds.), El inventario biológico del Canal de Panamá. II. Estudio ornitológico, herpetológico y mastozoológico, Panamá, pp. 107–159.
Ibáñez D., R., Jaramillo A., C.A., Solís, F.A. & Jaramillo, F.E. (1996) Inventario de anfibios y reptiles: Fase inicial para la conservacion de estas especies en el Parque Nacional Altos de Campana. Informe final del Proyecto No. G-9516. Circulo herpetologico de Panama, Panamá, 43 pp.
Ibáñez D., R., Solís, F.A., Jaramillo A., C.A. & Rand, A.S. (2001) An overview of the herpetology of Panama In: Johnson, J.D.; Webb, R.G.; Flores-Villela, O. (Eds.), Mesoamerican Herpetology: Systematics, Zoogeography, and Conservation, El Paso, Texas, pp. 159–170.
IUCN (2001) IUCN Red List Categories and Criteria: Version 3.1. IUCN Species Survival Commission, Gland, Switzerland and Cambridge, UK, ii + 30 pp. Available from http://www.iucnredlist.org/documents/redlist_cats_crit_en.pdf (accessed 14 June 2011).
Ivanova, N.V., De Waard, J. & Hebert, P.D.N. (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes, 6, 998–1002.
http://dx.doi.org/10.1111/j.1471-8286.2006.01428.xJansen, M., Bloch, R., Schulze, A. & Pfenninger, M. (2011) Integrative inventory of Bolivia’s lowland anurans reveals hidden diversity. Zoologica Scripta, 40, 567–583.
http://dx.doi.org/10.1111/j.1463-6409.2011.00498.xJaramillo A., C.A., Wilson, L.D., Ibáñez D., R. & Jaramillo, F.E. (2010) The herpetofauna of Panama: distribution and conservation status. In: Wilson, L.D.; Townsend, J.H.; Johnson, J.D.; Murphy, J.B. (Eds.), Conservation of Mesoamerican amphibians and reptiles. Eagle Mountain Press, Eagle Mountain, Utah, pp. 604–671.
Jarvis, A., Reuter, H.I., Nelson, A. & Guevara, E. (2006) Hole-filled seamless SRTM data V3. Available from http://srtm.csi.cgiar.org (accessed November 2009).
Köhler, G. (2003) Reptiles of Central America. First edition. Herpeton, Offenbach, 367 pp.
Köhler, G. (2008) Reptiles of Central America. Second edition. Herpeton, Offenbach, 400 pp.
Köhler, G. (2009) New species of Anolis formerly referred to as Anolis altae from Monteverde, Costa Rica (Squamata: Polychrotidae). Journal of Herpetology, 43, 11–20.
http://dx.doi.org/10.1670/07-180R2.1Köhler, G., Dehling, D.M. & Köhler, J.J. (2010) Cryptic species and hybridization in the Anolis polylepis complex, with the description of a new species from the Osa Peninsula, Costa Rica (Squamata: Polychrotidae). Zootaxa, 2718, 23–38.
Köhler, G., Sunyer, J., Ponce, M. & Batista, A. (2008) Noteworthy records of amphibians and reptiles in Panama (Amphibia: Plethodontidae, Craugastoridae, Hylidae; Reptilia: Polychrotidae). Senckenbergiana biologica, 88, 329–333.
Köhler, G., Batista, A., Vesely, M., Ponce, M., Carrizo, A. & Lotzkat, S. (2012) Evidence for the recognition of two species of Anolis formerly referred to as A. tropidogaster (Squamata: Dactyloidae). Zootaxa, 3348, 1–23.
Köhler, J.J., Hahn, M. & Köhler, G. (2012) Divergent evolution of hemipenial morphology in two cryptic species of mainland anoles related to Anolis polylepis. Salamandra, 48, 1–11.
Losos, J.B., Andrews, R.M., Sexton, O.J. & Schuler, A.L. (1991) Behavior, ecology, and locomotor performance of the giant anole, Anolis frenatus. Caribbean Journal of Science, 27, 173–179.
Lotzkat, S., Köhler, J.J., Hertz, A. & Köhler, G. (2010a) Morphology and colouration of male Anolis datzorum (Squamata: Polychrotidae). Salamandra, 46, 48–52.
Lotzkat, S., Stadler, L., Carrizo Diaz, A.R., Hertz, A. & Köhler, G. (2010b) Notes on the easternmost population of Diploglossus bilobatus (Squamata: Anguidae) in Veraguas, Panama. Salamandra, 46, 59–62.
Lotzkat, S., Bienentreu, J.-F., Hertz, A. & Köhler, G. (2011) A new species of Anolis (Squamata: Iguania: Dactyloidae) formerly referred to as A. pachypus from the Cordillera de Talamanca of western Panama and adjacent Costa Rica. Zootaxa, 3125, 1–21.
Lotzkat, S., Hertz, A. & Köhler, G. (2012a) A new species of Sibon (Squamata: Colubroidea: Dipsadidae) from the Cordillera Central of western Panama, with comments on other species of the genus in this area. Zootaxa, 3485, 26–40.
Lotzkat, S., Stadler, L., Batista, A., Hertz, A., Ponce, M., Hamad, N. & Köhler, G. (2012b) Distribution extension for Anolis gruuo Köhler, Ponce, Sunyer and Batista, 2007 (Reptilia: Squamata: Dactyloidae), in the Comarca Ngöbe-Buglé of western Panama, and first records from Veraguas province. Check List, 8, 620–625.
Martínez Cortés, V.C., Pimentel, N. & Hurdaneta, A. (1995 “1994”) Diversidad herpetofaunistica en los cerros “Narices" y "La Anselma”: Provincia de Veraguas. Distrito de Santa Fe. Scientia (Panamá), 9, 59–79.
Martínez Cortés, V.C. & Rodríguez, A. (1994 “1992”) Del primer inventario en "Cerro Tute". Amphibia: Caudata y Anura. Reptilia: Squamata. Sauria y Serpentes. Scientia (Panamá), 7, 29–53.
Myers, C.W. (1969) The ecological geography of cloud forest in Panama. American Museum Novitates, 2396, 1–52.
Myers, C.W. (1971) A new species of green anole (Reptilia, Sauria) from the north coast of Veraguas, Panama. American Museum Novitates, 2470, 1–14.
Myers, C.W. (1977) Anfibios y reptiles capturados en Fortuna, 1976. Revista Loteria, 254-255-256, 239–244.
Myers, C.W. & Duellman, W.E. (1982) A new species of Hyla from Cerro Colorado, and other tree frog records and geographical notes from Western Panama. American Museum Novitates, 2752, 1–32.
Myers, C.W., Williams, E.E. & McDiarmid, R.W. (1993) A new anoline lizard (Phenacosaurus) from the highland of Cerro de la Neblina, southern Venezuela. American Museum Novitates, 3070, 1–15.
Nicholson, K.E., Crother, B.I., Guyer, C. & Savage, J.M. (2012) It is time for a new classification of anoles (Squamata: Dactyloidae). Zootaxa, 3477, 1–108.
Nicholson, K.E., Glor, R.E., Kolbe, J.J., Larson, A., Hedges, S.B. & Losos, J.B. (2005) Mainland colonization by island lizards. Journal of Biogeography, 32, 1–10.
http://dx.doi.org/10.1111/j.1365-2699.2004.01222.xNicholson, K.E., Ibáñez D., R., Jaramillo A., C.A. & Lips, K.R. (2001) Morphological variation in the tropical anole, Anolis casildae (Squamata: Polychrotidae). Revista de Biologia Tropical, 49, 709–714.
Peters, J.A. & Donoso-Barros, R. (1970) Catalogue of the Neotropical Squamata. Part II: lizards and amphisbaenians. United States National Museum Bulletin, 297, 1–293.
http://dx.doi.org/10.5479/si.03629236.297.1Poe, S. (2004) Phylogeny of anoles. Herpetological Monographs, 18, 37–89.
http://dx.doi.org/10.1655/0733-1347(2004)018[0037:POA]2.0.CO;2Poe, S., Latella, I.M., Ryan, M.J. & Schaad, E.W. (2009) A new species of Anolis lizard (Squamata, Iguania) from Panama. Phyllomedusa, 8, 81–87.
Rand, A.S. & Myers, C.W. (1990) The herpetofauna of Barro Colorado Island, Panama: an ecological summary. In: Gentry, A.H. (Ed.), Four Neotropical rainforests. Yale University Press, New Haven, pp. 386–409.
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
http://dx.doi.org/10.1093/bioinformatics/btg180Sabaj Pérez, M.H. (2010) Standard symbolic codes for institutional resource collections in herpetology and ichthyology. an online reference. Verson 1.5 (4 Oct 2010). Available from http://www.asih.org/ (accessed 10 December 2010).
Savage, J.M. (1974) Type localities for species of amphibians and reptiles described from Costa Rica. Revista de Biologia Tropical, 22, 71–122.
Savage, J.M. (1997) On terminology for the description of the hemipenes of squamate reptiles. Herpetological Journal, 7, 23–25.
Savage, J.M. (2002) The amphibians and reptiles of Costa Rica. A herpetofauna between two continents, between two seas. University of Chicago Press, Chicago, xx+934 pp.
Savage, J.M. & Guyer, C. (1989) Infrageneric classification and species composition of the anole genera, Anolis, Ctenonotus, Dactyloa, Norops and Semiurus (Sauria: Iguanidae). Amphibia-Reptilia, 10, 105–116.
http://dx.doi.org/10.1163/156853889X00142Savage, J.M. & Talbot, J.J. (1978) The giant anoline lizards of Costa Rica and Western Panama. Copeia, 1978, 480–492.
http://dx.doi.org/10.2307/1443615Scott, N.J., Wilson, D.E., Jones, C. & Andrews, R. (1976) The choice of perch height dimensions by lizards of the genus Anolis (Reptilia, Lacertilia, Iguanidae). Journal of Herpetology, 10, 75–84. http://dx.doi.org/10.2307/1562787
Slevin, J.R. (1942) Notes on a collection of reptiles from Boquete, Panama, with the description of a new species of Hydromorphus. Proceedings of the California Academy of Sciences, 4th series, 23, 463–480.
Smithe, F.B. (1975–1981) Naturalist’s color guide. Part I. Color guide. 182 color swatches. American Museum of Natural History, New York.
Stadler, L. (2010) Diversität, Taxonomie und Zoogeographie der Herpetofauna der Umgebung von Alto de Piedra (Veraguas, Panama). Diploma thesis. Justus-Liebig-Universität, Gießen, 290 pp. Available from http://www.senckenberg.de/files/content/forschung/abteilung/terrzool/herpetologie/herpetofauna_alto_de_piedra_veraguas_panama_stadler_2010.pdf (accessed 05 March 2012).
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony methods. Molecular Biology and Evolution, 28, 2731–2739. http://dx.doi.org/10.1093/molbev/msr121
Talbot, J.J. (1974) Anolis chocorum Williams and Duellman, an addition to the lizard fauna of Costa Rica. Journal of Herpetology, 8, 256–257.
http://dx.doi.org/10.2307/1563177Taylor, E.H. (1956) A review of the lizards of Costa Rica. University of Kansas Science Bulletin, 38, 1–322.
Uetz, P. (2013) The Reptile Database. Available from http://www.reptile-database.org (accessed 20 January 2013).
Ugueto, G.N., Rivas, G., Barros, T. & Smith, E.N. (2009) A revision of the Venezuelan anoles II: redescription of Anolis squamulatus Peters 1863 and Anolis tigrinus Peters 1863 (Reptilia: Polychrotidae). Caribbean Journal of Science, 45, 30–51.
Vieites, D.R., Wollenberg, K.C., Andreone, F., Köhler, J., Glaw, F. & Vences, M. (2009) Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences of the United States of America, 106, 8267–8272.
http://dx.doi.org/10.1073/pnas.0810821106Williams, E.E. (1976) South American anoles: The species groups. Papéis Avulsos de Zoologia, 29, 259–268.
Williams, E.E. & Duellman, W.E. (1967) Anolis chocorum, a new punctatus-like anole from Darién, Panama (Sauria, Iguanidae). Breviora, 256, 1–12.
Young, B.E., Sedaghatkish, G., Roca, E. & Fuenmayor, Q.D. (1999) El estatus de la conservación de la herpetofauna de Panamá. Resumen del primer taller internacional sobre la herpetofauna de Panamá. The Nature Conservancy y Asociación Nacional para la Conservación de la Naturaleza (ANCON), Arlington, Virginia, 40 pp.