Check List 10(2): 388–391, 2014 © 2014 Check List and Authors Chec List ISSN 1809-127X (available at www.checklist.org.br) Journal of species lists and distribution

n A preliminary geographic distribution map of muiraquitan istributio D Nunes de Almeida & Toledo, 2012 (Amphibia: 1,2* 3 1 1

raphic , Rudolf von May and Andrew g WhitworthAnura: 1,2Microhylidae) eo Laura Allen , Jaime Villacampa Ortega , Oliver Burdekin G n o

1 The Crees Foundation. 7-8 Kendrick Mews. SW7 3HG. London, UK. otes 2 Institute of Biodiversity, Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow. G12 N 8QQ. Glasgow, UK. [email protected] 3 Museum of Vertebrate Zoology, University of California at Berkeley, 3101 Valley Life Sciences Building. 94720. Berkeley, CA, USA. * Corresponding author. E-mail: Abstract: Elachistocleis muiraquitan northwestern Brazil. Prior to the description of E. muiraquitan was recently described fromElachistocleis fifteen specimens bicolor, a species found at associated two sites with in Acre markedly state, , individuals fitting the description of this species found inE. muiraquitansoutheastern’s Peru potential and northwesterndistribution, based Bolivia on were known identified localities as along with climatic and environmental parameters. different habitat and environmental conditions. Here, we re-identified these specimens and also propose the first map of

Elachistocleis Parker, 1927 is a genus that has more than 900km away from the area where E. muiraquitan undergone much taxonomic revision in recent years. has been found, with major differences in climate and There are currently sixteen recognised species (De Sá et al. 2012; Pereyra et al. 2013), where half of which have range of E. bicolor covers an area of hot arid steppe and been described within the last three years. Prior to the vegetationwarm temperate between climates, the two while regions E. muiraquitan (IUCN 2012). is found The in an equatorial monsoon climate, with high temperatures any Elachistocleis presenting an immaculate venter was et al. 2006; World Meteorological designateddescription ofas fiveElachistocleis new species bicolor by Caramaschi Guérin-Meneville, (2010) 1838 (Duellman and Thomas 1996) or Elachistocleis ovalis specimensand rainfall of (Kottek E. bicolor and review reports by other Schneider, 1799. It has been argued that E. ovalis should be Organisation 2013). Our recent inspection of museum considered a nomen dubium Almeida and Toledo 2012; von May et al. 2008) suggest that De Sá et al. (2012) include E. ovalis as a valid species in previousresearchers records (Moravec of E. andbicolor Aparicio from southeastern2000; 2004; NunesPeru and de (Caramaschi 2010), although northwestern Bolivia represent E. muiraquitan. We revised as E. bicolor from southeastern Peru and northwestern their work. The records that we reviewed were identified in the Tambopata Province, Madre de Dios Department, E. ovalis that also come from the same locality in Peru specimens collected by John Cadle and Theodore Papenfuss Bolivia. We also evaluate two recordings identifiedE. bicolor as is distributed across southeastern South America, but not Peru and deposited at the Museum of Vertebrate Zoology (southeastern).in southeastern AccordingPeru and northwestern to Caramaschi Bolivia. (2010), In the light (MVZ) at the University of California, Berkeley, USA (MVZ of recent taxonomic evidence, there are several instances (173704, MVZ 173706, MVZ 103707, MVZ 199477 and E. bicolor being re- MVZ 199478 (Figure 1d); and specimens collected by RvM et al. 2012). The most recent example is inPermit Madre numbers de Dios, 008-2002-INRENA-J-DGFFS-DCB Peru) and theof populations description previously of a new Argentinian identified as Elachistocleis species Station,012-2003-INRENA-IFFSDCB, Manu Province, Madre issued de to DiosRvM for Department, collection (classifiedE. haroi; Pereyra(Giaretta et al. 2013). Peru and deposited in the at Museo the Los de Amigos Historia Biological Natural Nunes et al. (2012) recently described Elachistocleis muiraquitan, which has an immaculate venter and is distinguished from others in the genus by a light and Universidad Nacional Mayor de San Marcos, Peru (MUSM- merged mid-dorsal stripe running from the post cephalic body24224, length MUSM-24278, ratios described MUSM-24329). for E. muiraquitan. Measurements In terms of fold to the vent. It also has a longer head than any of the ofthe morphology specimens deposited and coloration at the allMVZ of match these the specimens, head to other species that lack ventral patterning. This species the description of E. muiraquitan. Photos of a specimen in Acre state, Brazil and to date there is no other published along with those from MUSM, have characteristics that fit informationwas described on fromthis species. fifteen specimensHere we present found newat two records sites under the name E. bicolor (photos 181 and 182 in von May ettaken al. 2010) at the represent Los Amigos E. muiraquitan.Biological Station An individual and published found distribution. of theThe species nearest andpart propose of the recognised the first maprange of of its E. potentialbicolor is E. muiraquitan at Romero Lodge, Madre de Dios, Peru, in 2012, was also identified as and is shown in Figures 1a, 1b 388 Allen et al. | Distribution map and biogeographical notes for Elachistocleis muiraquitan and 1c. Where we were unable to examine specimens from al. 2006, Raxworthy et al. 2007), such as the sample size some localities directly, we consulted other herpetologists for E. muiraquitan.

data, each focussing on a different environmental variable theworking calls of in E. the muiraquitan respective (Nunes occurrence de Almeida areas and to confirm Toledo Five pilot models were constructed using the WorldClim specimens’2012) and identification.E. bicolor Additionally, the similarity of contribution to each pilot model were used to construct a E. ovalis further(e.g. precipitation). model (Appendix Variables 1) (Baldwin with the and highest Bender per 2008). cent et al. 2002) suggests that recorded these are in all ‘ recorded of Tambopata’ individuals This model was jackknifed to assess variable importance of(Cocroft the same 2001) species. and These three in ‘Ranas calls de have Bolivia’ a frequency (Marquéz of and to point out highly correlated variables (Baldwin E. muiraquitan), whereas E. bicolor has a frequency of 5 kHz, to create a continuous logistic output of probability andapproximately call duration 4 kHz, of around with duration 2.5 seconds of 3 (Deto 4 la seconds Riva et (al. distribution.2009). The final The model average was bootstrapped training area (100 under replicates) curve 1996).

Elachistocleis species matched (AUC) value for the replicate runs in the receiver operator the The description map shown of in FigureE. muiraquitan 2 was created using localities characteristic (ROC) output was 0.991, showing a very where we confirmed that outputgood model was fit. processed in ArcGIS 10 using the maximum ; Hijmans et al.. 2005) Environmental and the To create a binary presence / absence map the factors were taken from WorldClim (version 1.4; http:// et al. 2013). There is evidence of some www.worldclim.org/ overpredictiontraining sensitivity and it plus should specificity be noted logistic the map threshold shows U.S. Geological Service (USGS), Global Forest Resource potential(Cao distribution and not realized distribution Assessment (FRA 2000; http://edc2.usgs.gov/glcc/fao/ (Phillips et al. index.php) and addedet al. to the modelling program MaxEnt shown(version to 3.3.3e; perform http://www.cs.princeton.edu/~schapire/ well at low sample sizes (Hernandez et uninhabited areas. 2006). Further work is required in maxent/; Phillips 2004, 2006). MaxEnt has been both sampling effort and identification of potentially Table 1. Details of records of Elachistocleis

specimens used to create the predicted range map shown in Figure 2. Abbreviations used for specimen numbers refer to the following collections: ZUEC = Museo de Zoologia ‘Prof. Adão José Cardoso’ Universidade Estadual de Campinas, Brazil; MUSM = ; CBF = Colecion Boliviana de Fauna, Instituto de Ecologia, Museo de la Historia Natural, La Paz, Bolivia; USNM = Smithsonian Institution, National Museum of Natural History; MVZ = Museum of Vertebrate Zoology at Berkeley, University of California; MCZ = Museum of Comparative Zoology, Harvard University; RMMU = Redpath Museum, McGill University. * Indicates records which have been confirmed as E. muiraquitan; the other specimens should be examinedORIGINAL for NAME further confirmation.SPECIMEN NUMBER LOCATION RECORD SOURCE Elachistocleis muiraquitan* Acre, Xapuri, Brazil Nunes et al. 2012 Elachistocleis muiraquitan* Rio Branco, Brazil Nunes et al. 2012 ZUEC 5666 78, Elachistocleis bicolor* von May et al. 2009 MUSM 24224, 242 Elachistocleis bicolor* Los Amigos Biological Station, Peru von May et al. 2009 24329 Elachistocleis bicolor* von May et al. 2009 Las Piedras Biodiversity Station, Peru Elachistocleis bicolor* von May et al. 2009 Cusco Amazónico, Peru Elachistocleis bicolor* von May et al. 2009 Cocha Cashu, Peru Elachistocleis bicolor* von May et al. 2009 Centro Sachavacayoc, Peru Elachistocleis bicolor* von May et al. 2009 Eco Amazonia, Peru Elachistocleis bicolor* von May et al. 2009 Explorer’s Inn, Peru Elachistocleis bicolor* Tambopata Center, Peru Elachistocleis bicolor* Riberalta, Bolivia Dahl et al. 2009 Romero Rainforest Lodge, Peru Andrew Whitworth, 6th October 2012 Elachistocleis bicolor* Moravec and Aparicio, 2000 Elachistocleis bicolor* Nacebe, Bolivia CBF (1) 6km NE of Riberalta, Bolivia Elachistocleis bicolor* Dahl et al. 2009 CBF (1) Moravec and Aparicio, 2004 Elachistocleis bicolor* Palmira, Bolivia Dahl et al. 2009 Sacrificio, Bolivia Elachistocleis bicolor* Dahl et al. 2009 Elachistocleis bicolor Balta, Peru Duellman and Thomas, 1996 Cobija, Bolivia Elachistocleis bicolor Smithsonian Museum Database Elachistocleis bicolor Smithsonian Museum Database USNM 247434 Explorer’s Inn, Peru Elachistocleis bicolor Smithsonian Museum Database USNM 247660 Explorer’s Inn, Peru Elachistocleis bicolor Smithsonian Museum Database USNM 343270 Explorer’s Inn Elachistocleis bicolor Smithsonian Museum Database USNM 343271 Explorer’s Inn Elachistocleis bicolor Smithsonian Museum Database USNM 343272 Explorer’s Inn Elachistocleis bicolor* USNM 343273 Explorer’s Inn Elachistocleis bicolor* MVZ 173704 Cusco Amazónico Albergue Lodge John E. Cadle Elachistocleis bicolor* MVZ 173706 Cusco Amazónico Albergue Lodge John E. Cadle Elachistocleis bicolor* Theodore J Papenfuss MVZ 173707 Cusco Amazónico Albergue Lodge John E. Cadle Elachistocleis bicolor* Theodore J Papenfuss MVZ 199477 Cusco Amazónico Albergue Lodge Elachistocleis bicolor MVZ 199478 Cusco Amazónico Albergue Lodge Elachistocleis ovalis MCZ A-88302 Cocha Cashu Dr Alan Ross Kiester Elachistocleis ovalis RMMU 1071 Cusco Amazónico Mark Chandler RMMU 1072 Cusco Amazónico Mark Chandler 389 Allen et al. | Distribution map and biogeographical notes for Elachistocleis muiraquitan

Figure 1. a) to c) In-life photos of Elachistocleis muiraquitan d) found at Romero Rainforest Lodge (-12°13′23.5914″ S, 70°58′50.505″ W), Madre de Dios, Peru on 6 October 2012 (photos by A. Whitworth). Specimens collected by John Cadle and Theodore Papenfuss deposited in the Museum of Vertebrate Zoology at the University of California, Berkeley (from left to right: MVZ 173704, MVZ 173706, MVZ 103707, MVZ 199477 and MVZ 199478).

Figure 2. Map showing locality records of Elachistocleis muiraquitan of the different environmental factors is detailed in Appendix 1. (as given in Table 1) and a potential predicted range using MaxEnt. The contribution

390 Allen et al. | Distribution map and biogeographical notes for Elachistocleis muiraquitan

Acknowledgments: its director Quinn Meyer for supporting the herpetological research as New World genera. BioMed Central Evolutionary Biology part of their conservationWe and first biodiversity of all thank monitoring The Crees programme. Foundation Also and frogs (Anura: ) with emphasis on relationships among Predicting species’ distributions from small numbers of12: occurrence 241. Pearson, R.G., C.J. Raxworthy, M. Nakamura, and A.T. Peterson.Journal 2007. of the University of Glasgow, especially Dr Ross MacLeod and Prof. Roger Biogeography Downie, for supporting fieldwork conducted in Peru. Thanks also to the records: A test case using cryptic geckos in Madagascar. andUniversidad also to the Nacional Ministerio Mayor de deAgricultura San Marcos of andPeru the for Museum providing of Vertebratethe permit species of Elachistocleis 34: 102–117. Zoology at Berkeley for providing a base to deposit valuable specimens Pereyra,Argentina. L.C., M.S.Zootaxa Akmentins, G. Laufer and M. Vaira. 2013. A new (Anura: Microhylidae) from north-western to conduct research in Peru. We also thank Chicago Herpetological 3694 (6): 525–544. Society, the Louise Hiom Fund and Glasgow Natural History Society for Phillips,Proceedings S.J., M. of Dudik the 21st and International R.E. Schapire. Conference 2004. A on maximum Machine Learning. entropy Bolivianfinancial specimens.support with RvM project thanks and Margarita field equipment. Medina-Müller We thank and Jiří NemesioMoravec approach to species distribution modelling; pp. 655–662, in: (National Museum, Prague, Czech Republic) for providing information on modellingNew York: ACMof species Press. geographic distributions. Ecological Modelling Carrillo for field assistance, the Amazon Conservation Association for Phillips, S.J., R.P. Anderson, and R.E. Schapire. 2006. Maximum entropy Programproviding in a Biology research (DBI-1103087). grant to work at Los Amigos Biological Station, and the National Science Foundation Postdoctoral Research Fellowship 190: 231–259. Literature Cited Raxworthy, C., C. Ingram, N. Rabibisoa, R. Pearson.Phelsuma 2007.) from Applications Madagascar. of EcologicalSystematic NicheBiology Modeling for Species Delimitation: A Review and research. Entropy Empirical Evaluation Using Day Geckos ( Baldwin, R.A. 2009. Use of maximum entropy modeling in wildlife 56(6): 907–923. Elachistocleis 11: 854–866. Journal of Wildlife Redpathbicolor Museum, occurrence McGill data. University Accessed 2013. through Museum Global of Biodiversity Vertebrate Baldwin,Management R.A. and Bender, L.C. 2008. Den-site characteristics of black Zoology, University of California, Berkeley 2013. bears in Rocky Mountain National Park, Colorado. 72(8): 1717–1724. SmithsonianInformation National Facility Museum Data portal. of Natural Accessible History at http://data.gbif.org/ 2013. Division of Cao, Y., DeWalt, R.E., Robinson, J.L., Tweddale, T., Hinz, L. and Passino, M. Amphibiansspecies/2421949/ and Reptiles. Captured Collections on 02. SeptemberAccessible at2013. selections.2013. Using Ecological Maxent toModelling model the historic distributions of stonefly species in Illinois streams: The effects of regularization andElachistocleis threshold http://collections. ovalis 259: 30–39. mnh.si.edu/search/herps/2010. Anfibios de Los Amigos,. Captured Manu y on Tambopata, 02 September Perú. 2013. Rapid Color Caramaschi,Elachistocleis U. 2010. Notes on the Taxonomic Status of Boletim von GuideMay, R., # 236,J.M. 12Jacobs, pl. R.D. Jennings, A. Catenazzi and L.O. Rodríguez. do Museu Schneider Nacional, 1799 Nova Série and descriptionZoologia of five new species of ElachistocleisParker 1927 (Amphibia:bicolor. Frogs Anura: of Tambopata, Microhylidae). Peru [Audio July 2013. The Field Museum, Chicago. Accessible at http:// 527: 1–30. fm2.fmnh.org/plantguides/guide_pdfs/236-10.pdf. Captured on 30 Cocroft, R. 2001. CD]. USA: Cornell Laboratory of Ornithology. von Status May, R.,of K. Siu-Ting, in J. Madre Jacobs, de M. Dios, Medina-Müller, Southern Peru. G. Herpetological Gagliardi, L. Dahl,tropical C., V. Novotny, and temperate J. Moravec communities. and S. Richards. Journal 2009. of Biogeography Beta Diversity of ConservationRodríguez and and M. BiologyDonnelly. 2009. Species Diversity and Conservation frogs in the forests of New Guinea, Amazonia and Europe: Contrasting Forest Resources De la Riva, I., R. Marquez and J. Bosch. 36(5): Assessment. 4(1): 14–29. 896–904. American Midland USGS Global Land Cover Characterization 2000. Naturalist 1996. Advertisement Calls of Four Accessible at http://edc2.usgs.gov/glcc/fao/index.php. Climatological information Duellman,Microhylid W. and Frogs R. Thomas. from Bolivia 1996. Anuran(Amphbia, Amphibians Anura). from a Seasonally forCaptured Rio Branco, July 2013. Brazil. Instituto Nacional de la Metereologia, Brasil. 136(2): 418–422. WorldAccessible Metereological at Organisation 2013. . Occasional Papers of the NaturalDry Forest History in Southeastern Museum, The PeruUniversity and Comparisons of Kansas of the Anurans http://worldweather.wmo.int/136/c01079.htm among sites in the Upper Amazon Basin. 2012. An acoustic Captured on 09 May 2013. evaluation of the geographical distribution of Elachistocleis180: 1–34. cesarii Giaretta, A., F. Silva de Andrade, I. Haga and D. Carvalho.Herpetology Notes Received: October 2013 Miranda-Ribiero 1920 (Anura: Microhylidae). The effect 5: Accepted: February 2014 of375–383. sample size and species characteristics on performance of different Published online: May 2014 Hernandez,species distributionP.A., Graham, modelling C.H., Master, methods. L.L., & Albert,Ecography D.L. 2006. Editorial Responsibility: Natan Medeiros Maciel

high resolution interpolated climate surfaces for global 29(5): land 773–785. areas. Hijmans,International R.J., S.E. Cameron,Journal of J.L.Climatology Parra, P.G. Jones and1978 A. Jarvis.. 2005. Very IUCN Red List of Threatened Species. Version 2012.2. Accessible Appendix 1. 25: 1965– IUCN 2012. permutation importanceA description of ofeach variable layer. layers used by MaxEnt to develop at http://www.iucnredlist.org/. Captured on 09 MayMeteorologische 2013. the predicted potential range in Figure 2 and the contribution and PERCENT PERMUTATION Kottek,Zeitschrift M., J. Grieser, C. Beck, B. Rudolf and F. Rubel. 2006. World Map VARIABLE of the Köppen-Geiger climate classification updated. Elachistocleis CONTRIBUTION IMPORTANCE bicolor. Guia 15(2): Sonora 259 de–263. las Ranas y Sapos de Bolivia. Alosa. Temperature seasonality 27.5 Marquéz,Moravec, R.,J. and I. De J. la Aparicio. Riva, J. Bosch 2000. and Amphibians E. Matheu. and 2002. reptiles recently (standard deviation *100) recorded from the surroundings of Riberalta (Departamento [Audio CD]. Beni, Average precipitation for April 40.1 Bolivia). Casopis Národního muzea Rada prirodovédná Average precipitation for 9.9 1 14.2 4.3 169(1-4): November 8.4 (Provincia–15. Abuna Departamento Pando, Bolivia). Casopis Národního Precipitation of driest month 7.2 1.5 Moravec,muzea J. Radaand J.prirodovédná Aparicio. 2004. Notes of the herpetofauna of Nacebe Global forest resources 6.9 0.7 Elachistocleis 173(1-4): Accessed 13 through–28. Global Biodiversity bicolor occurrence data. Average maximum temperature 6 6.2 Museum of Comparative Zoology, Harvard University 2013. forassessment May (FRA 2000) Information Facility Data portal. Accessible at http://data.gbif.org/ Average minimum temperature 3.1 species/2421949/Elachistocleis bicolor. Captured occurrence on 02 data. September Accessed 2013. through Global for December Museum of Vertebrate Zoology, University of California, Berkeley 2013. Slope 4.6 19.3 Minimum temperature of coldest 11.2 Biodiversity Information Facility Data portal. Accessible at http:// month 4.3 data.gbif.org/species/2421949/Elachistocleis . Captured on 02 September 2013. Average precipitation for May 2.93.4 15.7 NunesNorthern de Almeida, Brazil. Zootaxa C.H.L. and L.F. Toledo. 2012. A new species of Parker (Anura: Microhylidae) from the State of Acre, Mean temperature of warmest 1.9 0.6 3424: 43–50. quarter O de Sá, R., J. Streicher, R. Sekonyela, M. Forlani, S. Loader, E. Greenbaum, S. Richards and C. Haddad. 2012. Molecular Phylogeny of microhylid 391