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A new species of poison-dart frog (Anura: Dendrobatidae) from Manu province, Amazon region of southeastern Peru, with notes on its natural history, bioacoustics, phylogenetics, and recommended conservation status

SHIRLEY J. SERRANO-ROJAS, ANDREW WHITWORTH, JAIME VILLACAMPA, RUDOLF VON MAY, ROBERTO C. GUTIÉRREZ, JOSÉ M. PADIAL, JUAN C. CHAPARRO

Abstract


We describe and name a new species of poison-dart frog from the Amazonian slopes of the Andes in Manu Province, Madre de Dios Department, Peru; specifically within the Amarakaeri Communal Reserve and the buffer zone of Manu National Park. Ameerega shihuemoy sp. nov. is supported by a unique combination of characters: black dorsum with cream to light orange dorsolateral lines, blue belly reticulated with black, and the lack of axillary, thigh and calf flash marks. Within Ameerega, it shares the general appearance of A. altamazonica, A. boliviana, A. hahneli, A. ignipedis, A. petersi, A. picta, A. pongoensis, A. pulchripecta, A. simulans, A. smaragdina, and A. yungicola; each possessing a granular black to brown dorsum, a light labial bar, a conspicuous dorsolateral line running from the snout to the groin, and a metallic blue belly and underside of arms and hind limbs. From most of these species it can be distinguished by lacking flash marks on the axillae, thighs, and calves (absent in only A. boliviana and A. smaragdina, most A. petersi, and some A. pongoensis), by having bright cream to orange dorsolateral stripes (white, intense yellow, or green in all other species, with the exception of A. picta), and by its blue belly reticulated with black (bluish white and black in A. boliviana, green and blue with black marbling in A. petersi, and green and blue lacking black marbling in A. smaragdina). Its mating call also shows clear differences to morphologically similar species, with a lower note repetition rate, longer space between calls, and higher fundamental and dominant frequencies. Phylogenetic analyses based on the 16S mitochondrial rRNA fragment also support the distinctiveness of the new species and suggest that A. shihuemoy is most closely related to Ameerega macero, A. altamazonica, A. rubriventris, and two undescribed species (Ameerega sp. from Porto Walter, Acre, Brazil, and Ameerega sp. from Ivochote, Cusco, Peru). Genetically, the new species is most similar to the sympatric A. macero, from which it clearly differs in characteristics of its advertisement call and coloration. The new species is found near rocky streams during the dry season and near temporary water bodies during the rainy season. Tadpoles are found in lentic water along streams, or in shallow, slow-moving streams. Given its small geographic range, we recommend that A. shihuemoy should be considered 'Near threatened' (NT) according to IUCN Red List criteria.

 


Keywords


Amphibia, Advertisement call, Amarakaeri Communal Reserve, Ameerega, habitat, Manu Biosphere Reserve, premontane forest, rainforest, taxonomy

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References


Altig, R. & McDiarmid, R.W. (1999) Body plan: Development and Morphology. In: McDiarmid, R.W. & Altig, R. (Eds.), Tadpoles: The Biology of Anuran Larvae. The University of Chicago Press, pp. 24–51.

Altig, R. & Johnson, G.F. (1989) Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetological Monographs, 3, 81–109.

http://dx.doi.org/10.2307/1466987

Anderson, D.R., Burnham, K.P. & Thompson, W.L. (2000) Null hypothesis testing: problems, prevalence, and an alternative. The Journal of Wildlife Management, 64 (4), 912–923.

http://dx.doi.org/10.2307/3803199

Bartoń, K. (2014) MuMIn: Multi-model inference. R Package version 1.0. 0. Vienna, Austria: R Foundation for Statistical Computing. Available from: https://cran.r-project.org/package=MuMIn (Accessed 21 January 2015)

Bauer, L. (1986) A new genus and a new specific name in the dart poison frog family (Dendrobatidae, Anura, Amphibia). Ripa. Netherlands November, 1986, 1–12.

Bernal, M.H., Luna-Mora, V.F., Gallego, O. & Quevedo, A. (2007) A new species of poison frog (Amphibia: Dendrobatidae) from the Andean mountains of Tolima, Colombia. Zootaxa, 1638, 59–68.

Bibron, G. (1838)Batrachorum genera et species, Hylaplesia picta Bibr. Mus. Par. In: Tschudi, J.J. (Ed.) Classification der Batrachier mit Berücksichtigung der fossilen Thiere dieser Abtheilung der Reptilien. Neuchâtel, in der buchdruckerei von Petitpierre. pp. 1–99.

Bioacoustics Research Program (2011) Raven Pro: Interactive Sound Analysis Software (Version 1.4) [Computer software]. Ithaca, NY: The Cornell Lab of Ornithology. Available from: http://www.birds.cornell.edu/raven (accessed 02 January 2016)

Boulenger, G.A. (1883) On a collection of frogs from Yurimaguas, Huallaga River, Northern Peru. Proceedings of the Zoological Society of London, 51, 635–638.

http://dx.doi.org/10.1111/j.1469-7998.1883.tb06669.x

Boulenger, G.A. (1902) Descriptions of new batrachians and reptiles from the Andes of Peru and Bolivia. Journal of Natural History, 10 (59), 394–402.

http://dx.doi.org/10.1080/00222930208678691

Brotons, L., Thuiller, W., Araújo, M.B. & Hirzel, A.H. (2004) Presence-absence versus presence-only modelling methods for predicting bird habitat suitability. Ecography, 27 (4), 437–448.

http://dx.doi.org/10.1111/j.0906-7590.2004.03764.x

Brown, J.L., Schulte, R. & Summers, K. (2006) A new species of Dendrobates (Anura: Dendrobatidae) from the Amazonian lowlands in Peru. Zootaxa, 1152, 45–58.

Brown, J.L. & Twomey, E. (2009) Complicated histories: three new species of poison frogs of the genus Ameerega (Anura: Dendrobatidae) from north-central Peru. Zootaxa, 2049, 1–38.

Burnham, K.P. & Anderson, D.R. (2002) Model selection and multimodel inference. A practical information-theoretic approach. 2nd edn. Springer, New York, 488 pp.

Catenazzi, A., Lehr, E. & von May, R. (2013) The amphibians and reptiles of Manu National Park and its buffer zone, Amazon basin and eastern slopes of the Andes, Peru. Biota Neotropica, 13 (4), 269–283.

http://dx.doi.org/10.1590/s1676-06032013000400024

Chaparro, J.C. & Ochoa, J.A. (2005) Anfibios, reptiles y escorpiones registrados en Erika Lodge, Parque Nacional del Manu. Manu Ecological Adventures, 18 pp.

Chaparro, J.C., Alarcón, C., Condori, F.P. & Deichmann, J.L. (2016) Amphibians and Reptiles of the Amarakaeri Communal Reserve, Madre de Dios, Peru. Field Guides of the Field Museum of Chicago, USA. 766, 1–4. Available from: http://fieldguides.fieldmuseum.org/guides/guide/766 (accessed 01 September 2016)

Finer, M., Novoa, S. & Snelgrove, C. (2015) Deforestation Hotspots in the Peruvian Amazon, MAAP: 26. Available from: http://maaproject.org/2016/hotspots2015/ (accessed 17 June 2016)

Finer, M., Novoa, S. & Olexy, T. (2016) Construction of a New Highway between Manu National Park and Amarakaeri Communal Reserve (Madre de Dios), MAAP: 29. Available from: http://maaproject.org/2016/manu-road/ (accessed 17 June 2016)

Fox, J. & Weisberg, S. (2011) An {R} Companion to Applied Regression. 2nd edn. Thousand Oaks CA: Sage. Available from: http://socserv.socsci.mcmaster.ca/jfox/Books/Companion (accessed 25 February 2016)

Frost, D.R. (2016) Amphibian Species of the World: an Online Reference. Version 6.0. American Museum of Natural History, New York, USA. Electronic Database available from: http://research.amnh.org/herpetology/amphibia/index.html (accessed 10 June 2016)

Gosner, K.L. (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16 (3), 183–190.

Grant, T., Frost, D.R., Caldwell, J.P., Gagliardo, R., Haddad, C.F., Kok, P.J., Means, D.B., Noonan, B.P., Schargel, W.E. & Wheeler, W.C. (2006) Phylogenetic systematics of dart-poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae). Bulletin of the American Museum of Natural History, 299, 1–262.

http://dx.doi.org/10.1206/0003-0090(2006)299[1:PSODFA]2.0.CO;2

Haddad, C.F. & Martins, M. (1994) Four species of Brazilian poison frogs related to Epipedobates pictus (Dendrobatidae): taxonomy and natural history observations. Herpetologica, 50 (3), 282–295.

IUCN (2001) IUCN Red List Categories and Criteria. Version 3.1. IUCN Species Survival Commission, IUCN, Gland, Switzerland and Cambridge, UK. Available from: http://www.iucnredlist.org/info/categories_criteria2001 (accessed 20 February 2016)

Jackman, S. (2015) pscl: classes and methods for R developed in the political science computational laboratory. Stanford University. Department of Political Science, Stanford University. Stanford, California. R package version 1.4.9. Available from: http://pscl.stanford.edu/ (accessed 02 September 2016)

Jarvis, L.E., Angulo, A., Catenazzi, A., von May, R., Brown, J.L., Lehr, E. & Lewis, J. (2015) A re-assessment of priority amphibian species of Peru. Tropical Conservation Science, 8 (3), 623–645.

Lanfear, R., Calcott, B., Ho, S.Y. & Guindon, S. (2012) Partition Finder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular biology and evolution, 29 (6), 1695–1701.

http://dx.doi.org/10.1093/molbev/mss020

Laurance, W.F., Useche, D.C., Rendeiro, J., Kalka, M., Bradshaw, C.J., Sloan, S.P., Laurance, S.G. & Arroyo-Rodriguez, V. (2012) Averting biodiversity collapse in tropical forest protected areas. Nature, 489 (7415), 290–294.

http://dx.doi.org/10.1038/nature11318

Lötters, S., Debold, P., Henle, K., Glaw, F. & Kneller, M. (1997) Ein neuer Pfeilgiftfrosch aus der Epipedobates pictus-Gruppe vom Osthang der Cordillera Azul in Perú. Herpetofauna, 19 (110), 25–34.

Lötters, S. & Vences, M. (2000) Bermerkungen zur nomenklatur und taxonomie peruanischer Pfeilgiftfrösche (Anura: Dendrobatidae: Dendrobates, Epipedobates). Salamandra, 36 (4), 247–260.

Lötters, S., Schmitz, A. & Reichle, S. (2005) A new cryptic species of poison frog from the Bolivian Yungas (Anura: Dendrobatidae: Epipedobates). Herpetozoa, 18 (3), 115–124.

Lötters, S., Jungfer, K.H., Schmidt, W. & Henkel, F.W. (2007) Poison Frogs. Biology, Species & Captive Husbandry. Edition Chimaira, Germany, Frankfurt am Main, 667 pp.

Lötters, S., Schmitz, A., Reichle, S., Rödder, D. & Quennet, V. (2009) Another case of cryptic diversity in poison frogs (Dendrobatidae: Ameerega)—description of a new species from Bolivia. Zootaxa, 2028, 20–30.

McDiarmid, R.W. & Altig, R. (1999) Tadpoles: The Biology of Anuran Larvae. University of Chicago Press, Chicago, Illinois, U.S.A., 444 pp.

Museo Nacional de Ciencias Naturales (2016) Fonoteca Zoologica: an Online Reference, Madrid, Spain. Electronic Database available from: http//www.fonozoo.com (accessed 26 January 2016)

Myers, C.W., Rodriguez, L.O. & Icochea, J. (1998) Epipedobates simulans, a new cryptic species of poison frog from Southeastern Peru, with notes on E. macero and E. petersi (Dendrobatidae). American Museum Novitates, 3238, 1–20.

Pacheco-Suarez, M. (2015) Guía fotográfica de los anfibios de la región de los Yungas, Bolivia. Diversidad entre pendientes. Available from: https://diversidadentrependientes.files.wordpress.com/2015/09/guia-anfibios-pd1.pdf (accessed 1 December 2015)

R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available from: http://www.R-project.org/ (accessed 15 November 2015)

Roberts, J.L., Brown, J.L., von May, R., Arizabal, W., Schulte, R. & Summers, K. (2006) Genetic divergence and speciation in lowland and montane Peruvian poison frogs. Molecular Phylogenetics and Eevolution, 41 (1), 149–164.

http://dx.doi.org/10.1016/j.ympev.2006.05.005

Rodriguez, L. & Myers, C.W. (1993) A new poison frog from Manu National Park, southeastern Peru (Dendrobatidae, Epipedobates). American Museum Novitates, 3068, 1–15.

Santos, J.C., Coloma, L.A. & Cannatella, D.C. (2003) Multiple, recurring origins of aposematism and diet specialization in poison frogs. Proceedings of the National Academy of Sciences, 100 (22), 12792–12797.

http://dx.doi.org/10.1073/pnas.2133521100

Santos, J.C., Coloma, L.A., Summers, K., Caldwell, J.P., Ree, R. & Cannatella, D.C. (2009) Amazonian amphibian diversity is primarily derived from late Miocene Andean lineages. PLoS Biol, 7, e1000056.

http://dx.doi.org/10.1371/journal.pbio.1000056

Schulte, R. (1999) Pfeilgiftfrösche "Artenteil - Peru". Wailblingen, Germany, INBICO, 292 pp.

Silverstone, P.A. (1976) A revision of the poison-arrow frogs of the genus Phyllobates Bibron in Sagra (family Dendrobatidae). Science Bulletin. Natural History Museum of Los Angeles County, 53 pp.

Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22 (21), 2688–2690.

http://dx.doi.org/10.1093/bioinformatics/btl446

Symonds, R.E. & Moussalli, A. (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Behavioral Ecology and Sociobiology, 65 (1), 13–21.

http://dx.doi.org/10.1007/s00265-010-1037-6

Twomey, E. & Brown, J.L. (2008) A partial revision of the Ameerega hahneli complex (Anura: Dendrobatidae) and a new cryptic species from the East-Andean versant of Central Peru. Zootaxa, 1757, 49–65.

Vaz-Silva, W. & Medeiros Maciel, N. (2011) A new cryptic species of Ameerega (Anura: Dendrobatidae) from Brazilian Cerrado. Zootaxa, 2826, 57–68.

Vences, M., Kosuch, J., Boistel, R., Haddad, C.F., La Marca, E., Lötters, S. & Veith, M. (2003) Convergent evolution of aposematic coloration in Neotropical poison frogs: a molecular phylogenetic perspective. Organisms Diversity & Evolution, 3 (3), 215–226.

http://dx.doi.org/10.1078/1439-6092-00076

von May, R., Siu-Ting, K., Jacobs, J.M., Medina-Müller, M., Gagliardi, G., Rodríguez, L.O. & Donnelly, M.A. (2009) Species diversity and conservation status of amphibians in Madre de Dios, Perú. Herpetological Conservation and Biology, 4 (1), 14–29.

Whitworth, A. & Villacampa J. (2014) Amphibians of the Manu Learning Centre. Field guides of the Field Museum of Chicago, USA. 645, 1–7. Available from: http://fieldguides.fieldmuseum.org/guides/guide/645 (accessed 01 September 2016)

Whitworth, A., Downie, R., von May, R., Villacampa, J. & MacLeod, R. (2016a) How much potential biodiversity and conservation value can a regenerating rainforest provide? A 'best-case scenario' approach from the Peruvian Amazon. Tropical Conservation Science, 9 (1), 224–245.

Whitworth, A., Villacampa, J., Brown, A., Huarcaya, R.P., Downie, R. & MacLeod, R. (2016b) Past human disturbance effects upon biodiversity are greatest in the canopy; a case study on rainforest butterflies. PLOS ONE, 11 (3), e0150520.

http://dx.doi.org/10.1371/journal.pone.0150520




DOI: http://dx.doi.org/10.11646/zootaxa.4221.1.3

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