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
·: _ 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. Noble of the American Museum of Narural History, New York, was the first ro realize that dendrobatoids-which were then scattered among a number of families-form a narural group (Noble, 1926, 1931 ). He also proposed char they were nested among New World hyloids and most closely relared to the southeastern Brazilian frogs nO\\ recognized as Hylodidae.
~ 12 Taxonomy Recent Progress in the Systemat1cs of Poison Frogs and Their Relatives (Dendrobatoidea)
Noble's hypothesis was challenged by the British anatomist I. Griffiths (Griffilbs, 1959. 1963), who argued that dendrobaroids were nested among Old World ranoids and mosr clo~ely related to African frogs currently known ~ Arthroleptidae, Perropedetidae, and Phrynobatrachidae. Studies over the subsequent decades generally corroborated either Noble's (e.g., Lynch, 1971, 1973; Bogart, 1973) or Griffiths' (e.g., Duellman and Trucb, 1986; Ford, 1993; Ford and Cannatella, 1993; Gram eta/., 1997) scenarios.
With the addition of large amount~ of evidence from D A sequences (e.g. , Frost eta/., 2006; Granr n al., 2006) and morphology and behavior (Haas, 2003; Grant er a/., 2006), rhe weight of the evidence strongly corroborates Noble's hypothesis that dendrobaroids and hylodids are sister groups. In recognition of this, Gram n 11/. formally proposed the name Nobleobatia for the group of dendrobaroids and hylodids.
.... mily level Grouo"' As noted above, over the last few decades Oendrobaridae smsu faro grew from about 70 to 283 species, which is unwieldy and considerably larger than most nominal families in other verrebrare groups (e.g.• fishes and birds). Grant et a/. (2006) found dendrobaroids ro be monophyletic, bur also discovered that rhe species of dendrobaroids fall inro rwo large clades. One group included all of rhe poisonous ~pecies (as well as numerous non-poisonous species), whereas the other group consisted exclusively of (insofar as is known) non-roxie species. lhis allowed Granr tr ttl. (2006) to elevate rhe inclusive group of dendrobaroids ro rhe arbitrary rank of ~upcrfamily, Dendrobaroidea, and restrict Dendrobaridae ro rhe clade chat included rhe roxie species (thus retaining the popular association of the family name with poison frogs) and recognize a second family, Aromobatidae, for rhe other group. One could argue that srabilit) was threatened by the recognition of two families where once there was one. bur through observarion of the workings of the sysrematics wmmuniry ir is clear rhat parsing species inro more user-friendly units nor only invires additional research by other workers. ir provides a bener working framework for non-systematists than do very large raxa thar do nor focu~ on comparisons.
Wi thin these rwo families, Grant et al. (2006) also proposed ~everal subfamilies. WiLhin Dendrobatidae, rhey resurrected Colosrerhinae for the newly delimited or nJmed genera (see below for discussion of generic changes) Ameerega, Colostethus, Fpipedobates, and Silz•mtoneia; Hyloxalinae for the single genus HJ•loxalus; and Dendrobarinae for the genera most commonly recognized as poison or dan-poison frogs: Atklphobates, Dmdrobam, Mil~robates, Ooplmga, Ph).flobam, and Ranitomeya (and more recently Excrdobam Twome) and Brown, 2008a; see postscript). Within Aromobatidae, they nan1ed the new subfamily Anomaloglossinae for Anomaloglossus 'ld Rheobates; Aromobatinae for Aromobates and Aiamzophryne; and Allobarinae for rfJe single genus Alfobates.
r- Taxonomy 13 - c~
I Chapter 1
In addition ro facilirating taxonomy by grouping species imo more manageable evolutionary units, dividing dendrobatoids among these rwo families made for a geographically more coherenr view of diversiry than was previously available. Aromobatidae represents a predominandy cis-Andean radiation. Aromobatinae (Aromobates and Mannophryne) occurs only east of the Andes in Trinidad and Tobago, and Venezuela and adjacent Colombia; Rheobaus reaches only as far west as the eastern slopes of the Cordillera Cenrral of Colombia; Allobaw includes one species (A. chafcopis) on Marrinique and rwo com inenral species west of the Andes (see below) but is otherwise completely cis-Andean; and most of the diversity of Anomaloglossus occurs in Venezuela, with a handful of species found on the Pacific slopes of Colombia, Ecuador, and Panama. Dendrobatidae semu stricto continues to be a widespread dade, ranging from Nicaragua sourh to Bolivia and the Atlanric Coastal Forest of Brazil, although dendrobarid genera are confined within relatively clear geographic limits {see below).
The Colostethus Problem For decades it was widely recognized that Colosterlms was nor an evolutionary group, and identifying the distinct lineages confused under this name was one of the primary goals of the Gram et al. (2006) srudy. Steps toward resolving rhis problem were raken over a decade before by La Marca, who named Mannophryne La Marca, 1992. and Nephelobates LaMarca, 1994, for rwo predominandy Venezuelan groups then placed in ColostethttS. However, wirh the exccprion of the monorypic genus Aromoblltes, which was only discovered and named in 1991 (Myers et af., 1991 ), all of the other brown, cryptically colored species remained in Colostetlms. Prior to the revision by Grant et af. (2006), Colosmlms had grown to include nearly half the species in the (then) fam ily. As expected (e.g., Kaplan, 1997), Grant et al. found Colosmlms to be an artificial assemblage, although the extent of the non-monophyly was greater than had been anticipated, and it is in large parr for this reason that the taxonomy was revised so extensively (e.g., at the family level).
Grant et al. (2006) found rhe old Colostethus to be distributed among several distandy related lineages. Colosuthus semu stricto is restricted to a compact group of 21 species distributed in Central America, the Choc6 region of western Colombia, the Magdalena Valley in Colombia, and prcdominandy cloud-forest localities in the Andes of Colombia and Ecuador. No species of Colostetlms is known to be capable of sequestering lipophilic alkaloids, alrhough Daly rt a!. (1994) reponed rhat C. panamansis (as C. inguina/is; see Gram, 2004) posse~ses the water soluble alkaloid tetrodoroxin, and C. ucumari possesses a water soluble roxin of undetermined idenriry. Colostetlms is placed in Dendrobatidae within Colostethinae.
Most species of the former Colostetlms smsu !a to are disrribured between rwo distantly relared genera placed in differem families of dendrobaroids. Allobares includes 46 named species (Frost, 201 1), almost all of which occur east of the Andes. The only known exceptions ro this cis-Andean distribution are A. talamancae, which
- . I · :- 14 Taxonomy Recent Progress 1n the SystematiCS of Poison Frogs and The1r Relatives (Oendrobato1dea) occurs in Central America and extends south through rhe Choco co Ecuador, and A. niputidea from the Magdalena Valley in Colombia (Grant eta/., 2007). Wirhin this genus is a complex of superficially similar species traditionally placed in Silverstone's ( 1976) femora/is group (or directly in A. fomoralis), including A. femora lis, A. Ztlparo, A. myersi, and A. nifidus. Although ir was once believed rhat these species possessed defensive skin roxins. they do not appear ro be capable of sequestering alkaloids, and their exrensive morphological similarity to poisonous species of Dendrobatidae is probably due to mimicry. Also included in this genus are A. nidicola and A. chalco pis, which possess nidicolous and exoviviparous endouophic larvae, respectively. Given the diversiry of species in this clade (in terms of rhe number of species and their morphological, behavioral, and reproductive variarion), it is likely that further progress will allow additional clades in rhis group ro be recognized formally and for Allobares ro be resrricred to rhe fnnomlzs group. Al/obates is placed in Aromobatidae as the sole genus of the subsidiary subfamily Allobatinae.
The bulk (58 species) of rhe remaining species previously placed in Colostethw form an Andean radiation placed in Hyfoxttlus. A few species reach rhe Amazonian lowlands, but most occur at mid- ro high elevations. None of these species possesses a swollen third finger, which is mherwise found in some or all species of Allobam, Anoma/oglosms, and Colosrnbinae. \X'irhin Hyloxalus, the group of H. azureivemris, H. chloromzspedus, H. eleutherodacrylus, H. nexipus, and H. patitae is unusual among Hyloxalus in posse~sing a pale dorsolateral stripe, and most of these species arc brightly colored like the aposematic ~pedes. However, it has been demonstrated that H. azureiventris and H. chlorocraspedus lack skin roxins. Ir is 1herefore probable that this bright coloration i~ another insrance of Baresian mimicry within dendrobaroids. The name Cryproplrrllobar~s is available for this group, and it is likely that ir will be removed from rhe synonymy of Hyloxalus once our understanding of phylogeny impro\·es. Hyloxalus is placed in Dendrobatidae as the sole genus ofHyloxalinae.
The remaining species of the former Colostetlms form smaller groups. Anomalogfossus was named for rhe species that possess a median lingual process (Grant et aL, 1997) and includes 24 species, and Rheobates wa\ named for rhe Colombian species C palmatus and C pseudopalmatus. These genera are placed in Aromobatidae and together form Anomaloglo~sinae. Sift.ersron~ia was named for the nubicola group, which extends from Cemral America through much of the Choc6 region of Colombia. At present, only three species are included in rhis group; however, several additional species await description. Silz•mtoneia is placed in Dendrobaridae within Colosterhinae.
Of the two genera can·ed our of Coloswlms snzsu faro prior to rhe recent revision, Grant et al. (2006) corroborated the monophyly of La ~1arca's MannopJ,ryne, which currently includes 19 species. bur they found rharAromobatt'S noctunmsand Colostetlms saltuensis were nested within Nephelobates. Because the oldest available name for that group is AromobtzW, Nepl1t'lobttres is a junior synonym. and all of rhe species of Nephelobtttes were rransferred ro Aromobares, which is composed of 12 species. These rwo genera are placed in Aromobatidae and together form Aromobarinae.
Taxonomy 15 I r:f Olapter 1 .,... - ·s ous Ge p - N. noted above, all poisonous genera are placed in a restricted Dendrobatidae. HO\veYer, within rhis group, nor all poisonous genera are each other's closest relatives. Gram et a/. (2006) corroborated rhe findings of Sanros et al. (2003) and Vences flal. (2003) that the ability ro sequester lipophilic alkaloids evolved three rimes independently in this group. Gram et al. (2006) remicted Epipedobates to a small group of only seven species from the western Andes and adjacent Pacific lowlands (£. boulengeri also occurs on Gorgona Island off the Pacific coast of Colombia). Among rhese, it is nor clear if E. boulmgeri, £. darwinulflllnai, £. machalilla, or E. narinensis are capable of sequestering lipophilic alkaloids, but £. nmhonyi. £. espinosai, and E. rricolor are known to possess Lipophilic alkaloids in their defensive skin secretions. ~1ost of the species formerly known as Epipedobatrs (i.e., Epipedobaus smsu :-.1yers, 1987) are now placed in Ameerega. Ameerega includes 31 species, all of which are known or believed to secrete skin roxins. Most of these species are cis-Andean, the exceptions being A. mamlara and the presumed sister species A. andina and A. erythromos. The sister group of Ameer·ega is Cofostethus, which also includes at least rwo toxic species (Daly et nl., 1994; Gram, 2007). However, the roxie compounds in the dermal secretions of these species are soluble in water-the alkaloid teuodoroxin in C. pnnamnnsis and an undetermined compound in C. ummnri. The chemical differences between rhese compounds and rhe facr rhar none of the >250 species of alkaloid-possessing species of amphibians has been found to pos~e~ both classes of alkaloids are suggesth·e of independent uptake mechanisms. Amuregn, Colostetlms, and Epipedobmes together form the clade Colostethinae.
All orher poisonous species occur in Oendrobatinae, which does not include any species known ro Jack the ability ro sequester lipophilic alkaloids. These species are distributed among Adefphobntes (currently three Amazonian species}, Dendrobates (restricted ro the tinctorius group, from the lowlands east and west of the Andes), Minyobntes (monorypic, M. stqrrmarki, from Cerro Yapacana, Venezuela), Oophaga (the IJisrrionica group, from Central America and the Pacific lowlands of Colombia and nonhern Ecuador), Phyllobaus (identical to Phy/Jobaus smsu :-.1yers eta!., 1978, from Central America and the Pacific slopes of Colombia), RanitOIIIt')'ll (mosr species formerly placed in Minyobates and rhe z•mtrimnculata group). and Excidobmes, named by Twomey and Brown (2008a) for rhe western Amazonian species £. cnptil'IIS and E. mysterioms.
lncert~e <:edis and -om ·r c 1bi1 Of rhe 304 raxa mar were named in or subsequently transferred ro Oendrobaridae ar the rime of Grant et nl. (2006), five could not be placed and were considered tO be of uncertain placement or dubious srarus. These are (using rheir original genus names) Colosrnlms poecilonotus, C. ramirezi, Dendrobnres mysterioHts, Pbyllobates pmm1sis (which has been questioned for over a cenrury), and Prostbrrapis drmni. All other species were placed explicidy in rhe new raxonomy. In an important contribution, Twomey and Brown (2008a) resolved one of these problems by obraining and
·s; 16 Taxonomy Recent Progress in the Systematics of P01son Frogs and Their Relatives (Dendrobatoidea) analyzing DNA sequence data for Dendrobates mysteriosus, which rhey referred ro the newly named Excidobates.
""lle Direction of Systematic Research: What Can We Expect to Change? The new taxonomy of dendrobaroids proposed by Grant et al. (2006) is based on the analysis of an unprecedemed amoum of evidence bur is far from the last word on the systematics of this group. Twenty-nine species were named and referred ro their respective genera berween 2005 and 2010, and there is no evidence that the rare of species discovery is slowing. As noted above, Twomey and Brown (2008a) proposed Excidobates for E. captivus and E. mysteriosus. Subsequent phylogenetic analyses by Twomey and Brown (2008b), Brown et al. (2008a), Brown and Twomey (2009), ~ fanzanilla et al. (2009), and Perez-Pena eta!. (2010) increased the sampling density Jfkey groups and all recovered results rhar are consistent wirh the taxonomic changes proposed by Gram eta!. (2006) and Twomey and Brown (2008a), but new evidence and/or methods of inferring evolutionary relationships could, in principle, overturn .my part of the current taxonomy. For example, Samos et al. (2009) proposed al tered ~n er ic placemenrs for four species and, although they did not propose taxonomic changes to reflect their resulrs, found that Allobates alagoanus was sister of all other aromobacids (and nor closely related ro rhe remaining species of Allobates) and that ')aJt of Colostethus senm Grant eta!. (2006) was more closely related ro Ameerega than ro ocher species of Colostethus. lr is dear that the extent of our understanding va ries among groups, making it ?OSSible both ro identify groups especially in need of derailed investigation and co predict where changes ro rhe current mxonomy are most likely to occur. Although it >a priori ty ro discover evidence ro allow placemem of the four incertae sedis species 1... the new taxonomy, other areas of dendrobatid systematics have higher priority. ~ . ta.nr new species of dendrobarids await description, especially among the former (olostethus sensu lato, and it is critical that these species be formally named ro provide a.s complete a picture of the diversity of dendrobarids as possible. Having broken c~Lostethus sensu lato imo irs consricuenr lineages facilitates this endeavor greacly, as o.~e variation among species firs wi thin a phylogenecic framework and identifying <;:)Ccies for comparison is simplified. The rwo largest outstanding problems in ~de rsra nding phylogeny are Aflobares and Hyloxalus. Several conspicuous clades h.t•·e been idemified in both of these genera, and improved understanding of their re..ttionships to the other species placed in these genera will allow these and additional =;oups ro be recognized formally. Among the poisonous taxa, the placement of M·•1:robares steyermarki remains highly unstable (for conflicting placements see Grant a..;.,,, 2006; Twomey and Brown, 2008a; Brown eta!., 2008a; Santos et al., 2009; ;ez-Pena et al., 2010), and increased collecting and evidence from DNA sequences r~ shedding much needed light on the diversity and relationships of Ameerega and •tomeya (e.g., Brown et a!. , 2008a; Twomey and Brown, 2008b; Brown and 1i mey, 2009). We expect investigations by researchers over the next several years -....ke great progress in delimiting species and bringing additional evidence to bear
Taxonomy 17 {{E Chapter 1
on their phylogenetic relationships. resulting in an improved understanding of me systematics of these frogs.
Postscript As noted above, understanding of the systematics of poison frogs and their relatives is advancing rapidly, and in the months since this chapter was completed and submitted, the presem review of rhe literature has continued to swell. For the presenr purposes, unquestionably rhe most significant contribution is the collection of accounts published in Brown ~t nl. (2011) that revised me taxonomy of Ranitomeya. Ahhough their phylogenetic analysis was largely consistent with pre,'ious srudies, their gready expanded DNA sequence dataset (including 235 indh,iduals) and careful analysis of type specimens, newly collected material, and vocalizations allowed Brown et al. (2011) to correct numerous errors (e.g., clarification of the identity of Rcmitomeya ventrimaculata, treatment of R. mbrocephala as a nomen dubium) and refine the taxonomy of the clade. Brown eta!. (2011) restricted Ranitomeya to the 16 Amazonian species, which they distributed in four species groups, and in the same publication distributed the remaining 12 Andean and Central American species in three species groups in their newly proposed genus Andinobnus. Although many problems remain to be solved in dendrobatoid systematics, and no scientific srudy is ever the last word, this srudy is a major step forward and an exciting glimpse of the revisionary studies yer ro come.
Long thought lObe a morph of Oophaga klmanm rhi; 'mnningly ~o1orcd poison frog is now knu"n ro h~ a mnrph of Oopbtt.'(.ll hutrzmura
~ [; 18 Taxonom~ • Conservation International is a private, non-profit organization exempt from federal income tax under section 50 I c(3) of rhe I ncernal Revenue Code.
ISBN: 978- l-934151-27-3 © 2016 Conservation International All righ rs reserved.
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This guide is parr of the Conservation International Tropical Field Guide Series. The series editors are Russell A. Minermeier, Jose Vicenre Rodriguez-Mahecha, and Anthony B. Rylands.
Citation: Kahn, T.R., E. LaMarca, S. Loners, J.L. Brown, E. Twomey and A. Amezquita. Eds. 2016. Aposematic Poison Frr (Dendrobatidae) ofthe Andean Countries: Bolivia, Colombia, Ecwulor, Pmt and Venez11ela. Conservation lnrernarior Tropical Field Guide Series, Conservation International, Arlington. USA. xxiii + 588pp.
Example ofcitation for chapters and accounts: Brown, J. L. and E. Twomey. 2016. Yavari Poison Frog Ranitomrya yavaricola Perez-Pena, Chavez, Twomey, and Bro" 20 I 0. In: Aposematic Poisou Frogs (Dendrobatidae) ofthe Andtnn Countries: Bolivia, Colombia, Ecuador, Pml n Vmezuela, T.R. Kahn, E. LaMarca. S. Loners, J.L. Brown, E. Twomey and A. Amezquita (eds.), pp.519-5:! Conservation International Tropical Field Guide Series, Conservation lnrernational, Arlington. USA.
Printed in Bogota, Colombia by Union Grifica, Lrda.
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