CONSERVATION INTERNATIONAL TROPICAL FIELD GUIDE SERIES Aposematic Poison Frogs (Dendrobatidae) of the Andean Countries: Bolivia, Colombia, Ecuador, Peru and Venezuela H CH3 NOCH3 N O CH CH3 H3C 3 H H N N O HO Spiropyrrolizidine CH N 236A 3 H O O HO Batrachotoxin H Cl NH N Epibatidine Editors Ted R. Kahn Enrique La Marca Stefan Lötters Jason L. Brown Evan Twomey Adolfo Amézquita Illustrated by Ted R. Kahn Chapter 1 Recent Progress in the Systematics of Poison Frogs and Their Relatives (Dendrobatoidea) Taran Grant1 Darrel R. Frosr ~ IUSlll de /..oologia, Vniversicbdc de ao Paulo, S.io Paulo, Brazil '\ciemist Lmerit\15, American .Museum of Natural Hi,tory, ~e" York. l';Y, U~A llle fir~r steps in undemanding biodiversiry are ro idenrify species, which are the primary units of biodiversiry, and to group rhem in a way that informs subsequem studies in areas such a.o. ecology, conservation, and pharmacology, as well as funher re.~ea rch on their evolutionary relarionships. These are the tasks of sysremarics. Within systematics, the most basic level of research focuse~ on discovering species and elucidating their variation and distribution. Once species are idenrificd, they can be grouped based on any number of criteria, such as similariry, ecological affiniry, or geographic disrriburion. and rhere b no law prohibiting the use ofdifferent groupings ror differenr purposes. Howe,·er. because the biodiversity observed today was caused by evolution, eYolurionary relarion~hip~ provide rhe explanarory framework that unifies til areas of biology. Consequently. S)')temarisrs group species formally according tO heir relative recency of common evolutionary ancestry, or their phrlogeny. These phylogenetic groups, or clades, are named and, following rhe International Code of Zoological Nomenclature (ICZN, 1999), ranked as genera, families, and species. Rank-free systems of nomenclature have also been proposed, bur ro dare they have nm been widely applied: for argumcnrs and a promising alternative sec Kluge, 2005.) -\ point often overlooked br non-sprematistS is thar identif}•ing species and inferring r heir phylogenetic relatiomhips are highly theoretical and empirically challenging '~lentific problems. As evidence accumulates and knowledge increases, prior hvpotheses are corroborated or refuted, exisring names pass into and our ofsynonymy, C\\ species and clades are named, and species are shuffied among groups to reflect improved understanding of their relarionships. It is e.xpecrcd that taxo nomy will stable as evidence accumulates. However, to employ taxonomic stabiliry umo itself would compromise rhe scienrific srarus of systematics. Instead, te ~rabiliry can emerge only as rhe evidenrial basis for understanding ry relationships provides stable answers. It is frustrating and difficult for --.Ti;...c ..nd non-systematists alike tO keep up wirh the changing names, bur ri··e is ro employ a sraric cl~sificarion that obscures rhe growing body of knowledge behind a cloud of authoritarianism disguised as tradition or same roken, lhe very rules char promote progress in systematics can also r. The rule of priority establ ishes rhar the oldest available name that ,~ Taxonomy 9 '-G= I' Chapter 1 can be applied ro a given group musr be used. This rule encourages ~ciemists ro be the first co discover and name taxonomic groups in order co achieve the accolades that accompany these discoveries. ·n,e respecr and recognirion of fir~t discovery is one of the factors thar drive scienrisrs, and therefore science, forward. However, the technical requiremenrs for a new name ro be nomenclarurally valid are so lax rhar it is possible for non·specialists to have a detrimental impacr on systematics that is unparalleled in other sciences. Poison frogs are especially prone to this problem due ro rhe large number of cnrhusiasts who arc extremely knowledgeable abour the frogs bur lack the necessary rraining in systematics to allow them to quantify and analyze phylogenetic evidence ro substamiare changes ro raxonomy. Ir i~ therefore essemial rhat taxonomic proposals always be subjected ro peer review in \pecialized sc1enrific journals. Thb requirement of peer review in specialized journals is not a defense of rhe ivory tower. In the same way rhar an amateur asrronomer may discover a new star or galaxy and must have the right to report their discovery, a frog enthusiast may discover a new species or higher raxon and must have rhe righr ro publi~h their findings; however. in both cases the claims must be backed by scientific evidence, and the way chis is ensured is rhrough peer re,·iew in specialized journals. The difference is rhar astronomers are free ro ignore unsubsrantiared claims that are published without evidence or peer review (indeed, rhe rules of rhe Imernarional Asrronomical L:nion [I AU] are much more rigid than those rhar govern zoological name\), whereas systematisrs are required by rhe lnrernarional Code of Zoological l\omenclarure ro recognize rheir names, if nor rhe cnriries thar these names represenr. Over the pasr few decades the number of known species of poison frogs and rheir relatives has grown from around 70 ro 283 (host, 2011 ). As knowledge of rhe diversiry of the group has increased, rhere <llso has been a revolution in rhe \\a) systemarists approach the problem of inferring phylogeny. First, rigorously quanritative methods of analysb were developed (e.g.. Kluge and Farris, 1969; Farris, 1970), which allowed much of rhe subjectivity and aurhoritarianism rhar characteri7ed rhe sptemaric. of the Evolutionary Synthesis (e.g .. Huxley, 1940) ro be eliminared. "I he problem of inferring phylogenetic relarionships is among the most compurationally challenging cla!>ses of problems known, and new analytical tools and rheorctical approaches continue ro be developed (e.g., Huelsenbeck eta!., 2002; Drummond et a!., 2006; Starnatakis, 2006; Wheeler et nl., 2006; Goloboff eta!., 2008). Second, the genomic revolution has made ir possible for researchers ro obtain more data than they had dreamed possible only a decade ago. Datasers composed of hundreds of thousands and even millions of observariom are now common. As a re~ulr of the intensive srudies rhar have emerged from the~e advances, our undemanding of amphibian relationships has imprO\·ed significantly, and rhe raxonomy of several groups, including poison frogs, has been modified ro reflect rhese changes (e.g., Faivovich et ·: _ 10 Taxonomy Recent Progress in the Systematics of Poison Frogs and Their Relatives (Dendrobatoidea) al., 2005; Frost et al., 2006; Grant et al., 2006; Roelams et al., 2007; Hedges eta!., 2008; Van Bocxlaer et al., 201 0). Building on srudies carried out over the previous 15 years (e.g., Myers, 1991; Ford, 1993; Kaplan, 1997; Clough and Summers, 2000; Vences et al., 2000; Santos et a!., 2003; Vences et al., 2003), Gram et al. (2006) assembled a dataset composed of over 1.55 million base pairs (bp) of mirochondrial and nuclear DNA from 11 genes (approximately 6,100 bp: 1. = 3,740 bp per terminal), as well as 174 phenotypic characters scored from adult and larval morphology, alkaloid profiles, and behavior. These clara were sampled from 156 species of poison frogs and numerous close relatives. As a result of this srudy, Gram et al. (2006) overhauled the taxonomy of poison frogs in order ro reflect the increased knowledge of their phylogeny and ro incorporate several technically valid names that had been overlooked or dismissed by many workers. Additional progress was subsequendy achieved by Twomey and Brown (2008a) who ftmher modified the taxonomy based on rheir srudy of DNA sequence clara from previously unanalyzed species. ln rhe foUowing we briefly summarize rhe changes and highlight the areas of dart-poison frog systematics char are most in need Aromobatidae ~ ARheob~tes, JAnomaloglossinae ---c= noma1og ossus Allobates J Allobatinae Aromobates JAromobatinae Mannophryne --Colostethus 1 Ameerega . Epipedobatesj Colostethmae Silverstoneia Hyloxalus J Hyloxalinae / Phy/lobates Dendrobatidae Minyobates ,.--- Ranitomeya · · · · · · Excidobates Dendrobatinae Adelphobates Oophaga Dendrobate Figure 1.1. Phylogenetic relariomhip:s among genera of Dendrobatoidca. Relationships are has~d on Gram rt a/. (2001)) with the addition of E\'cidob,ues placed as rhe sister group of l?Jwitolllt')"tl following T"omcy md Bro\\n (:!008a). Andinolmm. described by Twomey, Brown, Amezquira, and ,\lejfa-\'arga> in Brown, Twomey, Ambquita, de Souza. Caldwell, U:itt~rs. von M.ty, :-., fdo-~ampaio. ~kjia-\'arg.ts, 1\~n:z-Pcria. Pepper, Poelm.m. Sanchez-Rodrigu~z. and Summers in 20 II is not included here. Taxonomy 11 ~ ~ I Chapter 1 of additional research. Figure 1.1 shows the phylogenetic relationships among the genera and higher raxa of dendrobawids and Table 1.1 gives the indented raxonomy. Table 1.1. The higher-level taxonomy of Dendrobatoidea Cope, 1865, following Grant eta/. (2006), Twomey and Brown (2008a) and Brown et at (2011) Family Subfamily Genus Aromobaridac Anomaloglossin ae AnomnlogLossus Grant et rd., 2006 Gram t't a/., 2006 Gram n nl., 2006 Rfgobnus Gram n nl., 2006 Aromobatinae Aromobnus Myers, DJ.Iy. and Paolillo. 1991 Gram n nl., 2006 Mnnnophrynt' LaMarca. 1992 Allobarinae Granr er A!klbntes Zimmerm;Ulll and Zimmermann, 1988 nl., 2006 Dendrobaridae Colosrethinae Cope. Amurega Bauer, 1986 Cope, 1865 1867 Colosuthus Cope. 1866 Eprpedobnus ~ lyer~. 198- Silt•t'rrtonein Gram rr a!.. 2006 I lyloxalinae Gram Hyloxalus Jimenez de Ia Espada, 187 1 " 1870" et rzl., 2006 Dendrobarinae Andinobtttes l\1·omey. Brown, Amezquita and Cope, 1865 ,\1ejia-Vargas in Brown tt al.. 2011 Ade/phobnres Gram n a!.. 2006 Dmdrobares \X'agler, 1830 £v:cidobates Twomey and Brown, 2008a Minyobatrs Myers, 1987 Oophngn Bauer, 1994 P/~y//obntes Dumcril and Bibron. 1841 Ra11itomrya Bauer. 1986 ~t e Ne ,... "-r 1t'cs n"'1'l+io..- · ... '"' '1e- ,.. ___ C' The placemenr of poison frogs relative to other groups of frog~ has been one of rhe most recalcitrant problems in amphibian systematics. Arguably the most important amphibian biologist of his generation, G.K.