geographical and altitudinal distribution of ... · 6 stcp engenharia de projetos ltda., curitiba,...

Submitted 24 September 2015Accepted 25 August 2016Published 4 October 2016

Corresponding authorMarcos R Bornscheinbornscheinmarcaogmailcom

Academic editorPhilippe Grandcolas

Additional Information andDeclarations can be found onpage 31

DOI 107717peerj2490

Copyright2016 Bornschein et al

Distributed underCreative Commons CC-BY 40

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Geographical and altitudinal distributionof Brachycephalus (AnuraBrachycephalidae) endemic to theBrazilian Atlantic RainforestMarcos R Bornschein12 Carina R Firkowski3 Ricardo Belmonte-Lopes234Leandro Correcirca2 Luiz F Ribeiro235 Seacutergio AA Morato6Reuber L Antoniazzi-Jr7 Bianca L Reinert28 Andreas LS Meyer34Felipe A Cini3 and Marcio R Pie234

1 Instituto de Biociecircncias Universidade Estadual Paulista Satildeo Vicente Satildeo Paulo Brazil2Mater NaturamdashInstituto de Estudos Ambientais Curitiba Paranaacute Brazil3Departamento de Zoologia Universidade Federal do Paranaacute Curitiba Paranaacute Brazil4Programa de Poacutes-Graduacatildeo em Zoologia Departamento de Zoologia Universidade Federal do ParanaacuteCuritiba Paranaacute Brazil

5 Escola de Sauacutede Pontifiacutecia Universidade Catoacutelica do Paranaacute Curitiba Paranaacute Brazil6 STCP Engenharia de Projetos Ltda Curitiba Paranaacute Brazil7Red de Ecoetologiacutea Instituto de Ecologiacutea AC Xalapa Veracruz Mexico8 Laboratoacuterio de Biodiversidade Conservacatildeo e Ecologia de Animais Silvestres Departamento de ZoologiaUniversidade Federal do Paranaacute Curitiba Paranaacute Brazil

ABSTRACTMountains of the Brazilian Atlantic Forest can act as islands of cold and wet climateleading to the isolation and speciation of species with low dispersal capacity suchas the toadlet species of the genus Brachycephalus This genus is composed primarilyby diurnal species with miniaturized body sizes (lt25 cm) inhabiting microhabitatsin the leaf litter of montane forests Still little is known about the geographicaldistribution altitudinal range and ecological limits of most Brachycephalus species Inthis study we review the available data on the geographical and altitudinal distributionof Brachycephalus based on occurrence records compiled from literature andmuseumsboth for the genus as a whole and separately for the three recently proposed groupsof species (ephippium didactylus and pernix) The final ensemble dataset comprised333 records 120 localities 28 described species and six undescribed ones Specieswere recorded in six relief units the richest of which being the Serra do Mar with 30species When the Serra do Mar is subdivided into three subunits Northern Centraland Southern Serra do Mar the number of species increase from north to the southwith records of six nine and 16 species respectively We were able to estimate theextent of occurrence of nearly half of the described species and the resulting estimatesindicate that many of them show remarkably small ranges some of which less than50 ha Brachycephalus species are present from sea level to roughly 1900 m asl withthe highest richness being found between 751 and 1000 m asl (21 spp) The specieswith the broadest altitudinal range were B didactylus (1075 m) and Brachycephalus sp1 (1035m) both in the didactylus group and B ephippium (1050m) of the ephippiumgroup The broadest altitudinal amplitude for species of the pernix group was recordedfor B brunneus (535 m) The lowest altitudinal records for the pernix group were at

How to cite this article Bornschein et al (2016) Geographical and altitudinal distribution of Brachycephalus (Anura Brachycephalidae)endemic to the Brazilian Atlantic Rainforest PeerJ 4e2490 DOI 107717peerj2490

845 m asl in the state of Paranaacute and at 455 m asl in the state of Santa CatarinaThe altitudinal occurrence in the pernix species group seems to decrease southwardSyntopy between species is also reviewed

Subjects Biodiversity Biogeography ZoologyKeywords Cloud forest Highlands Relief units Syntopy Species group Extent of occurrence

INTRODUCTIONBrachycephalus Fitzinger is a genus of miniaturized diurnal toadlets (usually lt25 cm insnout-vent length) that inhabit the forest floor of montane regions along the AtlanticRainforest of southeastern and southern Brazil (Izecksohn 1971 Giaretta amp Sawaya 1998Pombal Jr Wistuba amp Bornschein 1998 Napoli et al 2011 Pie et al 2013 see Rocha et al(2000) and Pombal Jr amp Izecksohn (2011) for reports of nocturnal activity) Brachycephaluspresents direct development and a reduction in the number and size of digits (Hanken ampWake 1993 Pombal Jr 1999 Yeh 2002) Some species are aposematic (yellow orangeor yellow with light red) of which some were confirmed as harboring neurotoxins(tetrodotoxin and analogues Sebben et al 1986 Pires Jr et al 2002 Pires Jr et al 2003Schwartz et al 2007)

Recently Kaplan (2002) proposed that the genus Psyllophryne Izecksohn should beconsidered as a junior synonym of Brachycephalus Psyllophryne included two speciesP didactyla and P hermogenesi lsquolsquowith dorsal surfaces brown tiny body sizes (snout-ventlength 86ndash102 mm) body leptodactyliform and long-distance jumpersrsquorsquo (Napoli et al2011) There are currently 29 described species of Brachycephalus (Frost 2015 see Pie ampRibeiro 2015 Ribeiro et al 2015) and although 20 of them were described within the last10 years it is likely that many more species are still waiting to be described Moreoverecological data on species of the genusBrachycephalus is still limited To date it only includesdata on the breeding behavior of B ephippium (Pombal Jr Sazima amp Haddad 1994 PombalJr 1999) vocal activity of B hermogenesi (Verdade et al 2008) advertisement calls of Bephippium (Pombal Jr Sazima amp Haddad 1994) B hermogenesi (Verdade et al 2008) Bpitanga (Arauacutejo et al 2012) B tridactylus (Garey et al 2012) and B crispus (Condez et al2014) abundance estimates of B didactylus (Van Sluys et al 2007 Almeida-Santos et al2011 Rocha et al 2013 Siqueira et al 2014) and its diet (Almeida-Santos et al 2011) thediet of B brunneus (Fontoura Ribeiro amp Pie 2011) B garbeanus (Dorigo et al 2012) andB pitanga (Oliveira amp Haddad 2015) and microhabitat preference of B garbeanus (Dorigoet al 2012)

A recently-proposed phylogenetic hypothesis for the genus indicated their separationinto three main clades with still some uncertainty regarding relationships within eachclade (Clemente-Carvalho et al 2011b) Based on the species studied by Clemente-Carvalho et al (2011b) one clade included B didactylus and B hermogenesi a secondclade included B brunneus B ferruginus B izecksohni B pernix and B pombali anda third clade included B alipioi B ephippium B garbeanus B nodoterga B pitangaB toby and B vertebralis Two morphological traitsmdashthe presenceabsence of dermal

Bornschein et al (2016) PeerJ DOI 107717peerj2490 241

co-ossification and body shapemdashwere used to distinguish three groups of species (Ribeiroet al 2015) namely ephippium didactylus and pernix groups The first was defined bythe presence of dermal co-ossification and bufoniform body shape and includes thefollowing species distributed in southeastern Brazil (from the state of Espiacuterito Santo southto the state of Satildeo Paulo) B alipioi B bufonoides B crispus B ephippium B garbeanusB guarani B margaritatus B nodoterga B pitanga B toby and B vertebralis (Ribeiro etal 2015) The didactylus group was defined by the absence of dermal co-ossification anda leptodactyliform body shape and includes B didactylus B hermogenesi and B pulex(Ribeiro et al 2015) Finally the pernix group was defined by the absence of dermalco-ossification and bufoniform body shape and includes the following species distributedin southern Brazil (states of Paranaacute and Santa Catarina) B auroguttatus B boticarioB brunneus B ferruginus B fuscolineatus B izecksohni B leopardus B mariaeterezaeB olivaceus B pernix B pombali B tridactylus and B verrucosus (Ribeiro et al 2015)Later an additional species from the pernix group was described from southern Brazil(Pie amp Ribeiro 2015) B quiririensis On the other hand the holotype of Brachycephalusatelopoides is currently missing (Pombal Jr 2010) and no population of this species innature is known Therefore given that diagnostic characters could not be inspectedB atelopoides was not assigned to any of the species groups (Ribeiro et al 2015) A recentstudy by Padial Grant amp Frost (2014) indicated that B hermogenesiwould be closely relatedto a species of the ephippium group implying that the didactylus and ephippium clades werenot monophyletic but the authors used the same dataset as the original Clemente-Carvalhoet al (2011b) study One possibility for this incongruence is that Padial Grant amp Frost(2014) only analyzed the concatenated dataset which could have masked variations amongdifferent among loci that were accounted for in species tree analyses by Clemente-Carvalhoet al (Ribeiro et al 2015)

An intriguing aspect of Brachycephalus is the high level of microendemism found inmost of its species For instance extensive field surveys often find species confined toone or a few adjacent mountaintops along the Atlantic Forest (Pie et al 2013) suggestingthat their diversification is strongly linked to the topographical characteristics of theirhabitats Therefore to understand the origin and distribution of Brachycephalus it iscrucial to integrate species occurrence data with the geographical attributes of the biomeswhere they are found The Atlantic Forest the second largest forested biome of SouthAmerica can be divided at least into eight broad relief units of which three correspondto higher altitude regions namely plateaus (lsquolsquoPlanaltosrsquorsquo) mountain ranges (lsquolsquoSerrasrsquorsquo)and escarpments (lsquolsquoEscarpasrsquorsquo) (IBGE 1993) The highest mountains of the AtlanticForest biome occur in the Serra da Mantiqueira and Serra do Mar Their formation isassociated with tectonic events dating back to the Paleocene which caused an uplift ofan eastern sector of southeastern Brazil and led to a depression in the eastern borderThis region was subsequently submerged by the ocean and led to the formation ofthe Santos basin (Almeida amp Carneiro 1998) A second downgrade occurred furtherinland establishing the Serra da Mantiqueira (it extends throughout the states of EspiacuteritoSanto Minas Gerais Rio de Janeiro and Satildeo Paulo Almeida amp Carneiro 1998) which iscurrently divided by the lsquolsquoParaiacuteba do Sulrsquorsquo river valley into northern and southern rims


(IBGE 1993 IBGE 2006 MMA 2016) The Serra do Mar formed between 300 and 400million years before present contitutes the new eastern border of the Brazilian plateau thatwas progressively eroded westward leaving remnants that formed coastal islands (Almeidaamp Carneiro 1998) This edge of the plateau called Serra do Mar was interrupted from thesouthern state of Satildeo Paulo by headward erosion of the Ribeira river valley and from itslower limit in northeastern state of Santa Catarina by headward erosion of the Itajaiacute Acuriver valley (Almeida amp Carneiro 1998)

Millions of years of erosion processes have shaped the escarpments and mountains ineastern and southern Brazil Instead of forming a continuous massif range several blocksof high elevation isolated by lower areas have been formed constituting a mountain rangeThese blocks receive one or more regional names of lsquolsquoSerrasrsquorsquo the highest of which beingSerra do Caparaoacute (2892 m asl) and Serra do Itatiaia (2791 m asl) both part of Serrada Mantiqueira The Serra do Mar in its northern limit (northern state of Rio de Janeiro)is characterized by several lsquolsquoSerrasrsquorsquo with the highest peak reaching up to 2230 m aslIts middle section presents a distinctive structure featuring a high plateau at the borderbetween the states of Rio de Janeiro and Satildeo Paulo which decreases in altitude southwarduntil southeast of Satildeo Paulo city In this region around the Satildeo Paulo city the Serra do Maris characterized as a border of the plateau (Almeida amp Carneiro 1998) reaching 800ndash900 masl whereas in the border between the states of Satildeo Paulo and Rio de Janeiro its altitudereaches up to 2050 m asl In the state of Paranaacute the Serra do Mar is characterized againby several lsquolsquoSerrasrsquorsquo with altitudes from 500 to 1000 m above the plateau (Maack 1981) thehighest peak reaches up to 1800 m asl (sensu Google Earth (satellite image from 2015)or 1922 m asl sensu Maack (1981)) The Serra do Mar in the state of Santa Catarina hasa very short extension (about 45 km in a northsouth straight line) The highest altitudesare found only near the border with the state of Paranaacute where it reaches up to 1524 mFurther south the Serra do Mar becomes increasingly lower reaching only sim600 m aslon the southern edge of occurrence of this relief unit

Themountainous regions of the Atlantic Forest might have contributed to the formationand distribution limits of Brachycephalus in several ways For instance mountains couldhave supported population remnants of many species during warmer periods throughoutthe Quaternary (eg Carnaval et al 2009 Brunes et al 2010 Thomeacute et al 2010 Amaro etal 2012 see also Wollenberg et al 2011 Paacuteez-Moscoso amp Guayasamin 2012 and GiarlaVoss amp Jansa 2014 for similar scenarios in other montane regions) mainly due to theirdistinctly colder and wetter climatic conditions Hence they played an important rolein the diversification of animals with low dispersion capacities including certain birds(Mata et al 2009) and amphibians (Cruz amp Feio 2007 Brunes et al 2010 Thomeacute et al2010) This has been confirmed in an investigation of the environmental niches of differentBrachycephalus species groups given that they were shown to occupy distinct regions ofclimatic space (Pie et al 2013) That analysis included most of the described species (aswell some that were undescribed) and was based occurrence records associated with speciesdescriptions museum specimens and a few comprehensive references They have alsopresented new geographical distribution limits for the genus and records of altitude for


all species However no study to date has explored explicitly the altitudinal variation andprovided estimates of geographical distributions of Brachycephalus species

Understanding the ecological limits geographical distributions and altitudinal ranges ofBrachycephalus species is of considerable importance particularly to direct more effectiveconservation actions In the present study we address the aforementioned aspects byreviewing the geographical and altitudinal distribution of Brachycephalus based on recordscompiled from literature and museum specimens In particular expanding a previouseffort by Pie et al (2013) we now include the entire literature on Brachycephalus whichnearly tripled the number of sources in relation to that study We analyze the geographicaldistribution and altitudinal amplitude of occurrence of the genus as a whole as well asseparately based on their species groups

MATERIALS AND METHODSSpecies recordsIn an earlier paper (Pie et al 2013) occurrence records of Brachycephalus species wereobtained from the SpeciesLink portal (wwwsplinkorgbr) as well as from DZUP (Colecatildeode Herpetologia Departamento de Zoologia Universidade Federal do Paranaacute state ofParanaacute Brazil) and MHNCI (Museu de Histoacuteria Natural Capatildeo da Imbuia - PrefeituraMunicipal de Curitiba) collections and from the species descriptions themselves For thispaper we expanded that dataset by compiling additional records from DZUP and froma broader review of the literature A few unpublished records obtained by the authorsin southern Brazil were also included to improve the dataset Collection handling andpreservation permits were issued by ICMBIO (22470ndash1 and 22470ndash2) We carried out thesame careful analysis as in Pie et al (2013) to check the precise geographical coordinatesof point records using topographic maps (at different scales) resources of the GoogleEarth software including the titles of photographs associated with different locationsand descriptive information of localities in other publications The final dataset usedfor the analyses included only those records which coordinate precision index value wasbetween 11 and 30 according to McLaren et al reprinted in Knyazhnitskiy et al (2000)To help further revisions we also listed occurrence records considered imprecise after ourrevision (see lsquoResultsrsquo) Although there are methods for georeferencing imprecise locations(eg Wieczorek Guo amp Hijmans 2004) we preferred to discard the records that did notmeet these standards

Altitudinal records were either compiled from the literature or when that informationwas unavailable by plotting occurrence records on Google Earth The altitudinal range ofsome species were obtained directly from the literature or from the field by the authorsThe altitudinal range represents the lower and higher altitudinal occurrence record of aspecies in a given locality Although some records had precise locations they were locatedon slopes where the exact altitude of the record was difficult to ascertain and therefore wereomitted from further analysis but not from the compiled table to assist future revisions

All records were associated with Brazilian relief units (MMA 2016) by simply plottingeach record against a map of the limits of different relief units In two of the major relief


units we also analyzed our data separately for their subunits as follows the Serra daMantiqueira as lsquolsquoNorthern Serra da Mantiqueirarsquorsquo (states of Espiacuterito Santo and adjacentMinas Gerais) and lsquolsquoSouthern Serra daMantiqueirarsquorsquo (states ofMinas Gerais Rio de Janeiroand Satildeo Paulo) and the Serra doMar as lsquolsquoNorthern Serra doMarrsquorsquo (state of Rio de Janeiro)lsquolsquoCentral Serra do Marrsquorsquo (southern state of Rio de Janeiro and state of Satildeo Paulo) andlsquolsquoSouthern Serra do Marrsquorsquo (southern state of Satildeo Paulo and states of Paranaacute and SantaCatarina) The Serra da Mantiqueira we subdivided into two sectors because this unitcomprises naturally two sectors isolated by the lsquolsquoParaiacuteba do Sulrsquorsquo relief unit (IBGE 1993IBGE 2006 MMA 2016) The Serra do Mar we subdivided into sectors according to theinterruption of escarpments (IBGE 2006) Geographical coordinates are based into theWGS84 datum

Geographical distribution measurementWe tentatively provide estimates of species geographical distributions as their lsquolsquoextentof occurrencersquorsquo sensu IUCN (2012) using two methods The first is an adaptation oflsquolsquominimum convex polygonrsquorsquo (Mohr 1947) as Reinert Bornschein amp Firkowski (2007)which allowed for changing the shape of the minimum convex polygon whenever it waspossible to remove areas that are obviously unsuitable for the persistence of the species suchas cities plantations bodies of water and vegetation in the early stages of regeneration aswell areas beyond the altitudinal amplitude record of the species In the second method wemade polygons by considering the lowest altimetric quota with records of the species whilealso omitting unsuitable areas (as above) We made these environmental and altitudinalassessments and produced the resulting polygons using Google Earth Pro 7141529 Wethen measured the areas encompassed by each polygon using GEPath 145 Althoughwe disregarded unsuitable areas when drawing the polygons we treated the resultingmeasurements as lsquolsquoextent of occurrencersquorsquo and not lsquolsquoarea of occupancyrsquorsquo (sensu IUCN 2012)because microhabitat requirements can prevent the species from occurring in some partsof the area within the polygons Unfortunately we were unable to determine occurrencepolygons of many species when the abovementioned criteria led to obviously unrealisticdistribution polygons primarily for the following reasons (1) when there were exceedinglyfew records that were usually very scattered andor encompassed vast degraded areas or(2) when the altitudinal range of occurrence of a species based on their altitudinal limitsencompassed unreasonably large areas (usually heading west)

Species groupsAll described species in the present compilation were assigned to one of the threespecies groups by Ribeiro et al (2015) except for B atelopoides (see above) The presentcompilation also includes some undescribed species not yet assigned to one of the threegroups all of them were mentioned as new species or potentially new species in therespective source of their records Two of them were here assigned to the ephippium groupbecause they probably represent populations of B ephippium that could be split into twospecies one of which from the state of Rio de Janeiro (Siqueira Vrcibradic amp Rocha 2013see also Siqueira et al 2011) and the other from the state of Satildeo Paulo (Pie et al 2013)


Table 1 Records of Brachycephalus spp Altitude is provided in meters (above sea level)

Speciesa Relief unitsb Groupc Localityd State Altitude Source e

B didactylus NorthernSerra da Man-tiqueira

didactylus Monumento Natural Serra das Torres(2100prime04primeprimeS 4113prime17primeprimeW) municipalityof Atiacutelio Vivaacutecqua

ES (600ndash900) Oliveira et al (2012) Oliveira et al (2013)

B didactylus Northern Serrado Mar

didactylus Fazenda Santa Baacuterbara (2225prime17primeprimeS4235prime01primeprimeW) Parque Estadual dos TrecircsPicos municipality of Cachoeiras deMacacu

RJ 500ndash800 Siqueira et al (2009)Almeida-Santos et al (2011)


didactylus Reserva Ecoloacutegica de Guapiacu(2224prime00primeprimeS 4244prime00primeprimeW) municipalityof Cachoeiras de Macacu

RJ 300ndash520 Siqueira et al (2014)


didactylus Reserva Ecoloacutegica Rio das Pedras(2259prime00primeprimeS 4406prime45primeprimeW) municipalityof Mangaratiba

RJ 200ndash1110 This study Carvalho-e-Silva Silva amp Carvalho-e-Silva (2008) Almeida-Santos et al (2011)Rocha et al (2013)


didactylus Sacra Famiacutelia do Tinguaacute (2229prime11primeprimeS4336prime18primeprimeW) municipality ofEngenheiro Paulo de Frontin

RJ 600 Izecksohn (1971) Pombal Jr (2001)Ribeiro Alves amp Haddad (2005)Alves et al (2006) Alves et al (2009) SilvaCampos amp Sebben (2007) Verdade et al (2008)Clemente-Carvalho et al (2009) Campos (2011)Pombal Jr amp Izecksohn (2011) Pie et al (2013)


didactylus Theodoro de Oliveira (first position2222prime11primeprimeS 4233prime25primeprimeW) ParqueEstadual dos Trecircs Picos municipality ofNova Friburgo

RJ (1100ndash1400) This study Siqueira et al (2011)


didactylus Tinguaacute (2235prime51primeprimeS 4324prime54primeprimeW) mu-nicipality of Nova Iguacu

RJ 35 Izecksohn (1971)


didactylus Vila Dois Rios (2311prime01primeprimeS 4412prime23primeprimeW)Ilha Grande municipality of Angra dosReis

RJ 220ndash240 This study Rocha et al (2000)Rocha et al (2001) Van Sluys et al (2007)

B hermogenesi Central Serrado Mar

didactylus Corcovado (2328prime08primeprimeS 4511prime29primeprimeW)municipality of Ubatuba

SP (70) Giaretta amp Sawaya (1998) Verdade et al (2008)


didactylus Estacatildeo Bioloacutegica de Boraceacuteia (first posi-tion 2339prime10primeprimeS 4553prime05primeprimeW) munici-pality of Salesoacutepolis

SP 900 Pimenta Beacuternils amp Pombal Jr (2007)Verdade et al (2008)


didactylus Fazenda Capricoacuternio (2323prime27primeprimeS4504prime26primeprimeW) municipality of Ubatuba

SP 60 Giaretta amp Sawaya (1998) Verdade et al (2008)


didactylus Picinguaba (2322prime21primeprimeS 4449prime53primeprimeW)Parque Estadual da Serra do Marmunicipality of Ubatuba

SP 0ndash700 Giaretta amp Sawaya (1998) Pimenta Beacuternilsamp Pombal Jr (2007) Verdade et al (2008)Clemente-Carvalho et al (2009) Pie et al (2013)

(continued on next page)

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Table 1 (continued)



didactylus Reserva Bioloacutegica do Alto da Serrade Paranapiacaba (2346prime40primeprimeS4618prime45primeprimeW) municipality of SantoAndreacute

SP (800) Verdade et al (2008)


didactylus Reserva Florestal de Morro Grande(2342prime08primeprimeS 4658prime22primeprimeW) municipalityof Cotia

SP (990) Dixo amp Verdade (2006) Verdade et al (2008)

B pulex Preacute-Litoracircneas didactylus Serra Bonita (1523prime28primeprimeS 3933prime59primeprimeW)municipality of Camacan

BA 800ndash930 Napoli et al (2011)

Brachycephalussp 1

Paranapiacaba didactylus Caratuval (2451prime17primeprimeS 4843primeprime43primeprimeW)near the Parque Estadual das Lauraacuteceasmunicipality of Adrianoacutepolis

PR 900 Firkowski (2013 withoutspecies identification)Pie et al (2013 as lsquolsquoBrachycephalus sp nov 1rsquorsquo)

Brachycephalussp 1

Paranapiacaba didactylus Caratuval (2451prime14primeprimeS 4842prime01primeprimeW)Parque Estadual das Lauraacuteceas munici-pality of Adrianoacutepolis

PR 890 Pie et al (2013 as lsquolsquoBrachycephalus sp nov 1rsquorsquo)

Brachycephalussp 1

Paranapiacaba didactylus Fazenda Primavera (2453prime08primeprimeS4845prime51primeprimeW) municipality of Tunasdo Paranaacute


Brachycephalussp 1

Paranapiacaba didactylus Fazenda Thalia (2530prime58primeprimeS4940prime12primeprimeW) municipality of BalsaNova

PR 1025 Firkowski (2013 without species identification)Pie et al (2013 as lsquolsquoBrachycephalus sp nov 1rsquorsquo)

Brachycephalussp 1

Paranapiacaba didactylus Base of the Serra Aacutegua Limpa(2428prime52primeprimeS 4847prime12primeprimeW) municipalityof Apiaiacute

SP 920 This study DZUP Firkowski (2013 withoutspecies identification)

Brachycephalussp 1

Southern Serrado Mar

didactylus Alto Quiriri (2605prime34primeprimeS 4859prime41primeprimeW)municipality of Garuva

SC 240 Pie et al (2013 as lsquolsquoBrachycephalus sp nov 1rsquorsquo)

Brachycephalussp 1


didactylus Castelo dos Bugres (first position2613prime47primeprimeS 4903prime20primeprimeW) municipalityof Joinville

SC 790ndash860 Pie et al (2013 as lsquolsquoBrachycephalus sp nov 1rsquorsquo)

Brachycephalussp 1


didactylus Colocircnia Castelhanos (2547prime58primeprimeS4854prime40primeprimeW) municipality of Guaratuba

PR 290 Cunha Oliveira amp Hartmann (2010 aslsquolsquoBrachycephalus aff hermogenesirsquorsquo)Oliveira et al (2011 as lsquolsquoB hermogenesirsquorsquo)Pie et al (2013 as lsquolsquoBrachycephalus sp nov 1rsquorsquo)

Brachycephalussp 1


didactylus Corvo (2520prime17primeprimeS 4854prime56primeprimeW)municipality of Quatro Barras


Brachycephalussp 1


didactylus Dona Francisca (2609prime52primeprimeS4859prime23primeprimeW) municipality of Joinville


Brachycephalussp 1


didactylus Estrada do rio do Juacutelio (2617prime02primeprimeS4906prime08primeprimeW) municipality of Joinville

SC 650 Mariotto (2014 as lsquolsquoBrachycephalus sprsquorsquo)

Brachycephalussp 1


didactylus Fazenda Pico Paranaacute (2513prime29primeprimeS4851prime17primeprimeW) municipality of CampinaGrande do Sul



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Table 1 (continued)


Brachycephalussp 1


didactylus Mananciais da Serra (2529prime29primeprimeS4858prime40primeprimeW) municipality of Piraquara

PR 1050 This study DZUP Pie et al (2013 aslsquolsquoBrachycephalus sp nov 1rsquorsquo)

Brachycephalussp 1


didactylus Pico Agudinho (2536prime24primeprimeS4843prime33primeprimeW) Serra da Pratamunicipality of Morretes


Brachycephalussp 1


didactylus Recanto das Hortecircncias (2533prime24primeprimeS4859prime38primeprimeW) municipality of Satildeo Joseacutedos Pinhais

PR 975 This study DZUP

Brachycephalussp 1


didactylus Reserva Particular do PatrimocircnioNatural Salto Morato (2510prime00primeprimeS4817prime21primeprimeW) municipality ofGuaraquecaba

PR 45ndash900 This study Pereira et al (2010 aslsquolsquoB hermogenesirsquorsquo) Santos-Pereira et al (2011as lsquolsquoB hermogenesirsquorsquo)

Brachycephalussp 1


didactylus Siacutetio Ananias (2547prime08primeprimeS 4843prime03primeprimeW)municipality of Guaratuba


Brachycephalussp 1


didactylus Truticultura (2601prime33primeprimeS 4852prime02primeprimeW)municipality of Garuva


B alipioi NorthernSerra da Man-tiqueira

ephippium Fazenda Aoki or Fazenda dos Japoneses(2028prime24primeprimeS 4100prime36primeprimeW) boundary ofthe municipalities of Vargem Alta andDomingos Martins

ES 1070ndash1100 Pombal Jr amp Gasparini (2006)Clemente-Carvalho et al (2009)Clemente-Carvalho et al (2011b)Clemente-Carvalho et al (2012)Pombal Jr amp Izecksohn (2011) Pie et al (2013)


ephippium Forno Grande (2031prime41primeprimeS 4106prime51primeprimeW)Parque Estadual de Forno Grande mu-nicipality of Castelo

ES (1430) Pie et al (2013)

B bufonoides Northern Serrado Mar

ephippium Serra de Macaeacute (2218prime02primeprimeS4218prime20primeprimeW) municipality of NovaFriburgo

RJ (1100) Miranda-Ribeiro (1920) Pombal Jr (2010)Pombal Jr amp Izecksohn (2011)

B crispus Central Serrado Mar

ephippium Bacia B Nuacutecleo Cunha ParqueEstadual da Serra do Mar (2315prime15primeprimeS4501prime58primeprimeW) municipality of Cunha

SP 800-1100 Condez et al (2014)

B ephippium NorthernSerra da Man-tiqueira

ephippium Serra do Pai Inaacutecio (2048prime13primeprimeS4229prime07primeprimeW) Parque Estadual daSerra do Brigadeiro boundary of themunicipalities of Ervaacutelia and Miradouro

MG (1350) Pombal Jr amp Izecksohn (2011)

B ephippium SouthernSerra da Man-tiqueira

ephippium Condomiacutenio Ermida (2314prime13primeprimeS4658prime52primeprimeW) Serra do Japi municipalityof Jundiaiacute

SP 1225 Pie et al (2013)


ephippium Hotel Fazenda Peacute da Serra (2251prime56primeprimeS4531prime40primeprimeW) municipality ofPindamonhangaba

SP 700 Pie et al (2013)


ephippium Lago Azul (2227prime23primeprimeS 4436prime34primeprimeW)Parque Nacional do Itatiaia municipalityof Itatiaia

RJ 750 Pie et al (2013)


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Table 1 (continued)



ephippium Maromba (2225prime43primeprimeS 4437prime11primeprimeW)Parque Nacional do Itatiaia municipalityof Itatiaia

RJ 1125 Pie et al (2013)


ephippium Monteiro Lobato (2257prime07primeprimeS4550prime20primeprimeW) municipality of MonteiroLobato

SP 700 Pombal Jr amp Izecksohn (2011)


ephippium Observatoacuterio de Capricoacuternio(2253prime54primeprimeS 4649prime01primeprimeW) Serradas Cabras Joaquim Egiacutedio Districtboundary of the municipalities ofCampinas and Morungaba

SP 1085 Pombal Jr (1999) Pombal Jr Sazima amp Had-dad (1994) Pombal Jr amp Izecksohn (2011)Pie et al (2013)


ephippium Parque Municipal de Itapetinga (GrotaFunda) (2311prime07primeprimeS 4631prime47primeprimeW) mu-nicipality of Atibaia

SP 900ndash1250 Giaretta (1999) Giaretta et al (1999)Clemente-Carvalho et al (2009)Clemente-Carvalho et al (2011b)Pie et al (2013)


ephippium Reserva Bioloacutegica da Serra do Japi(2317prime07primeprimeS 4700prime05primeprimeW) Serra do Japiboundary of the municipalities of Jundiaiacuteand Cabreuacuteva

SP 1000 Giaretta et al (1997) Pombal Jr amp Izeck-sohn (2011) Clemente-Carvalho et al (2009)Clemente-Carvalho et al (2016) Pie et al (2013)


ephippium Reserva Ecoloacutegica do Trabiju(2248prime01primeprimeS 4532prime03primeprimeW) Trabijumunicipality of Pindamonhangaba

SP (1000) Pombal Jr amp Izecksohn (2011)


ephippium Reserva Pedra Branca (2256prime22primeprimeS4541prime04primeprimeW) municipality of Tremembeacute



ephippium Santo Antocircnio do Pinhal (2249prime28primeprimeS4540prime20primeprimeW) municipality of Santo An-tocircnio do Pinhal



ephippium Satildeo Francisco Xavier (2253prime44primeprimeS4558prime04primeprimeW) municipality of Satildeo Joseacutedos Campos

SP 1000 Clemente-Carvalho et al (2008)Clemente-Carvalho et al (2011a)Clemente-Carvalho et al (2016)Pombal Jr amp Izecksohn (2011)Pie et al (2013)


ephippium Serra Negra (2157prime28primeprimeS 4347prime20primeprimeW)municipality of Santa Baacuterbara do MonteVerde

MG Campos (2011 as lsquolsquoBMVMG2rsquorsquo)

B ephippium Paraiacuteba do Sul ephippium Serra da Concoacuterdia (2220prime30primeprimeS4344prime04primeprimeW) Parque Estadual Serrada Concoacuterdia Baratildeo de Juparanatildemunicipality of Valenca

RJ (900) Pombal Jr amp Izecksohn (2011)

B ephippium Northern Serrado Mar

ephippium Alto do Soberbo (2227prime15primeprimeS4259prime21primeprimeW) municipality ofTeresoacutepolis

RJ 1250 Pombal Jr amp Izecksohn (2011)


Bornschein

etal(2016)PeerJDO

I107717peerj24901041

Table 1 (continued)



ephippium Comary (2227prime22primeprimeS 4258prime24primeprimeW) mu-nicipality of Teresoacutepolis



ephippium Floresta dos Macacos (2258prime15primeprimeS4315prime24primeprimeW) municipality of Rio deJaneiro



ephippium Garrafatildeo (2228prime04primeprimeS 4301prime52primeprimeW) mu-nicipality of Guapimirim



ephippium Pedra Branca (2255prime55primeprimeS 4328prime23primeprimeW)Serra da Pedra Branca municipality ofRio de Janeiro

RJ 1000 Pombal Jr (2001) Pombal Jr amp Izecksohn (2011)


ephippium Represa do Rio Grande (2255prime58primeprimeS4326prime36primeprimeW) Parque Estadual da PedraBranca municipality of Rio de Janeiro

RJ (150) Pombal Jr amp Izecksohn (2011) Pie et al (2013)


ephippium Reserva Ecoloacutegica Rio das Pedras(2259prime00primeprimeS 4406prime45primeprimeW) municipalityof Mangaratiba

RJ 200-1110 Carvalho-e-Silva Silva amp Carvalho-e-Silva(2008)


ephippium Riacho Beija-flor (2227prime04primeprimeS4300prime04primeprimeW) Parque Nacional da Serrados Oacutergatildeos municipality of Teresoacutepolis

RJ 1195 Pie et al (2013)


ephippium Rocio District (2228prime23primeprimeS 4314prime38primeprimeW)municipality of Petroacutepolis

RJ 950 Pie et al (2013)


ephippium Serra do Tinguaacute (2235prime31primeprimeS4328prime16primeprimeW) municipality of NovaIguacu



ephippium Vale da Revolta (2226prime17primeprimeS4256prime19primeprimeW) municipality ofTeresoacutepolis



ephippium Varginha (2224prime34primeprimeS 4252prime11primeprimeW) mu-nicipality of Teresoacutepolis


B ephippium Central Serrado Mar

ephippium Bonito (2242prime51primeprimeS 4434prime39primeprimeW) Serrada Bocaina municipality of Satildeo Joseacute doBarreiro



ephippium Estacatildeo Ecoloacutegica de Bananal(2248prime05primeprimeS 4422prime12primeprimeW) Serra daBocaina municipality of Bananal

SP (1200) Zaher Aguiar amp Pombal (2005)


ephippium Liacutedice District (2250prime01primeprimeS 4411prime32primeprimeW)municipality of Rio Claro

RJ (650) Pombal Jr (2001) Pombal Jr amp Izecksohn (2011)


ephippium Pedra Branca (2310prime38primeprimeS 4447prime19primeprimeW)Serra da Bocaina municipality of Parati



ephippium Peniacutensula do Bororeacute (2347prime11primeprimeS4638prime45primeprimeW) Represa Billings GrajauacuteDistrict municipality of Satildeo Paulo

SP 780 Pie et al (2013 as lsquolsquoBrachycephalus nodotergarsquorsquo)Abbeg et al (2015 as lsquolsquoclearly refers to anotherspecies (than B nodoterga of Pie et al 2013)rsquorsquo)


Bornschein

etal(2016)PeerJDO

I107717peerj24901141

Table 1 (continued)



ephippium Reserva Florestal de Morro Grande(2342prime08primeprimeS 4658prime22primeprimeW) municipalityof Cotia

SP (990) Dixo amp Verdade (2006)

B garbeanus Northern Serrado Mar

ephippium Alto Caledocircnia (2220prime10primeprimeS4233prime20primeprimeW) municipality of NovaFriburgo



ephippium Baixo Caledocircnia (2221prime33primeprimeS4234prime12primeprimeW) municipality of NovaFriburgo

RJ 1600ndash1900 Pombal Jr amp Izecksohn (2011)Siqueira et al (2011)Siqueira Vrcibradic amp Rocha (2013)Dorigo et al (2012)


ephippium Macaeacute de Cima (2221prime37primeprimeS4217prime50primeprimeW) municipality of NovaFriburgo

RJ 1130 Clemente-Carvalho et al (2008 aslsquolsquoB ephippiumrsquorsquo) Clemente-Carvalho et al(2009 as lsquolsquoB ephippiumrsquorsquo)Clemente-Carvalho et al (2011b)Clemente-Carvalho et al (2011a lsquolsquobrsquorsquo aslsquolsquoB ephippiumrsquorsquo) Pombal Jr amp Izecksohn(2011) Pie et al (2013)


ephippium Morro Satildeo Joatildeo (2222prime47primeprimeS4230prime34primeprimeW) municipality of NovaFriburgo






ephippium Serra Nevada (2221prime46primeprimeS 4232prime48primeprimeW)municipality of Nova Friburgo



ephippium Theodoro de Oliveira (second position2221prime48primeprimeS 4233prime13primeprimeW) ParqueEstadual dos Trecircs Picos municipality ofNova Friburgo

RJ 1400 Pombal Jr amp Izecksohn (2011)Siqueira et al (2011)Siqueira Vrcibradic amp Rocha (2013)

B guarani Central Serrado Mar

ephippium Morro Prumirim (2320prime50primeprimeS4501prime37primeprimeW) municipality of Ubatuba

SP 500ndash900 Giaretta (1999 altitude determined byClemente-Carvalho et al (2012))Clemente-Carvalho et al (2012)Condez et al (2014)

B margarita-tus

Northern Serrado Mar

ephippium Castelo Country Club (2232prime21primeprimeS4313prime08primeprimeW) municipality of Petroacutepolis


B margarita-tus


ephippium Castelo Montebello (2224prime24primeprimeS4258prime06primeprimeW) municipality ofTeresoacutepolis


B margarita-tus


ephippium Independecircncia (2232prime58primeprimeS4312prime27primeprimeW) municipality of Petroacutepolis


B margarita-tus


ephippium Morro Azul (2228prime34primeprimeS 4334prime40primeprimeW)municipality of Engenheiro Paulo deFrontin

RJ 620 Campos (2011 as lsquolsquoBPF RJ2rsquorsquo)Pombal Jr amp Izecksohn (2011)


Bornschein

etal(2016)PeerJDO

I107717peerj24901241

Table 1 (continued)


B margarita-tus


ephippium Quitandinha (2231prime47primeprimeS 4312prime26primeprimeW)municipality of Petroacutepolis


B margarita-tus


ephippium Sacra Famiacutelia do Tinguaacute (2229prime11primeprimeS4336prime18primeprimeW) municipality ofEngenheiro Paulo de Frontin

RJ 600 Izecksohn (1971 as lsquolsquoB ephippiumrsquorsquo)Pombal Jr (2001 as lsquolsquoBrachycephaluscf ephippiumrsquorsquo) Pombal Jr amp Izecksohn (2011)Pie et al (2013 as lsquolsquoB ephippiumrsquorsquo)

B nodoterga Central Serrado Mar

ephippium Estacatildeo Bioloacutegica de Boraceacuteia (secondposition 2338prime00primeprimeS 4552prime00primeprimeW) mu-nicipality of Salesoacutepolis

SP 945 Pombal Jr Wistuba amp Bornschein (1998)Pombal Jr (2001) Pombal Jr (2010)Ribeiro Alves amp Haddad (2005)Alves et al (2006) Alves et al (2009)Haddad et al (2010)Pombal Jr amp Izecksohn (2011) Pie et al (2013)Abegg et al (2015)Clemente-Carvalho et al (2016)


ephippium Fazenda Paiva Ramos (2328prime21primeprimeS4647prime25primeprimeW) Serra de Satildeo Roquemunicipality of Osasco

SP 820 Abegg et al (2015)


ephippium Pico do Ramalho (2351prime42primeprimeS4521prime28primeprimeW) Ilha de Satildeo Sebastiatildeomunicipality of Ilhabela

SP 700ndash900 Ribeiro (2006 as lsquolsquoBrachycephalus sp affnodotergarsquorsquo) Pombal Jr amp Izecksohn (2011)Pie et al (2013) Abegg et al (2015)Clemente-Carvalho et al (2016)


ephippium Serra da Cantareira (2327prime13primeprimeS4638prime11primeprimeW) Parque Estadual daCantareira municipality of Satildeo Paulo

SP (850) Miranda-Ribeiro (1920)Ribeiro Alves amp Haddad (2005) Alves et al(2006) Alves et al (2009)Clemente-Carvalho et al (2009)Clemente-Carvalho et al (2011b)Clemente-Carvalho et al (2012)Clemente-Carvalho et al (2016)Haddad et al (2010) Pombal Jr (2010)Pombal Jr amp Izecksohn (2011)Condez et al (2014) Abegg et al (2015)

B pitanga Central Serrado Mar

ephippium Fazenda Capricoacuternio (2322prime36primeprimeS4504prime07primeprimeW) municipality of Ubatuba

SP (450) Alves et al (2009) Campos Silva amp Sebben(2010 as lsquolsquoBrachycephalus sp 2rsquorsquo)Campos (2011) Pie et al (2013)


ephippium Nuacutecleo Santa Virgiacutenia (2319prime23primeprimeS4505prime19primeprimeW) Parque Estadual da Serrado Mar municipality of Satildeo Luis doParaitinga

SP 980ndash1140 Oliveira (2013) Tandel et al (2014)Oliveira amp Haddad (2015)


ephippium SP 125 - municipality of Satildeo Luiacutes doParaitinga (2322prime57primeprimeS 4509prime59primeprimeW)

SP 935ndash950 This study DZUP


Bornschein

etal(2016)PeerJDO

I107717peerj24901341

Table 1 (continued)



ephippium Trilha do Ipiranga 50 m from the Rio Ipi-ranga (2320prime39primeprimeS 4508prime16primeprimeW) Nuacute-cleo Santa Virgiacutenia Parque Estadual daSerra do Mar municipality of Satildeo Luisdo Paraitinga

SP 900ndash960 Alves et al (2009)Clemente-Carvalho et al (2009)Clemente-Carvalho et al (2011b)Arauacutejo et al (2012) Oliveira (2013)Pie et al (2013)

B toby Central Serrado Mar

ephippium Morro do Corcovado (2327prime20primeprimeS4511prime49primeprimeW) Parque Estadual da Serrado Mar municipality of Ubatuba

SP 750 Haddad et al (2010)Clemente-Carvalho et al (2011b)Clemente-Carvalho et al (2012)Pie et al (2013) Condez et al (2014)

B vertebralis Central Serrado Mar

ephippium Morro Cuzcuzeiro (2318prime03primeprimeS4447prime30primeprimeW) Nuacutecleo Picinguaba ParqueEstadual da Serra do Mar municipalityof Ubatuba

SP 900 Clemente-Carvalho et al (2011b) Pie et al(2013) Condez et al (2014)



RJ (630) Pombal Jr (2001) Pombal Jr (2010)Clemente-Carvalho et al (2009)Pie et al (2013)

Brachycephalussp 2


ephippium Theodoro de Oliveira (first position2222prime11primeprimeS 4233prime25primeprimeW) ParqueEstadual dos Trecircs Picos municipality ofNova Friburgo

RJ 1100ndash1200 Siqueira et al (2011 as lsquolsquoBrachycephalus sprsquorsquo)(Siqueira Vrcibradic amp Rocha 2013as lsquolsquoBrachycephalus sp novrsquorsquo)

Brachycephalussp 3

Central Serrado Mar

ephippium Paranapiacaba (2346prime30primeprimeS4617prime57primeprimeW) municipality of SantoAndreacute

SP 825 Pombal Jr amp Izecksohn (2011 as lsquolsquoBephippiumrsquorsquo) Pie et al (2013 aslsquolsquoBrachycephalus sp 1rsquorsquo )

Brachycephalussp 3

Central Serrado Mar

ephippium Parque Natural Municipal Nascentesde Paranapiacaba (2346prime10primeprimeS4617prime36primeprimeW) municipality of SantoAndreacute

SP (800ndash1164) Trevine et al (2014 as lsquolsquoBrachycephalus sprsquorsquo)

Brachycephalussp 3

Central Serrado Mar

ephippium Reserva Bioloacutegica do Alto da Serrade Paranapiacaba (2346prime40primeprimeS4618prime45primeprimeW) municipality of SantoAndreacute

SP 800 Pie et al (2013 as lsquolsquoBrachycephalus sp 1rsquorsquo)

B aurogutta-tus


pernix Pedra da Tartaruga (2600prime21primeprimeS4855prime25primeprimeW) municipality of Garuva

SC 1070ndash1100 This study DZUP Firkowski (2013 withoutspecies identification) Ribeiro et al (2015)

B boticario Leste Catari-nense

pernix Morro do Cachorro (2646prime42primeprimeS4901prime57primeprimeW) boundary of themunicipalities of Blumenau Gasparand Luiz Alves


B brunneus Southern Serrado Mar

pernix Camapuatilde (2515prime59primeprimeS 4850prime16primeprimeW)Serra dos Oacutergatildeos boundary of the mu-nicipalities of Campina Grande do Suland Antonina

PR 1595 Fontoura Ribeiro amp Pie (2011) Firkowski(2013 without species identification)Pie et al (2013)


Bornschein

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I107717peerj24901441

Table 1 (continued)



pernix Caranguejeira (2520prime27primeprimeS 4854prime31primeprimeW)Serra da Graciosa municipality of Qua-tro Barras

PR 1095ndash1110 This study DZUP Firkowski (2013 withoutspecies identification)


pernix Caratuva (2514prime33primeprimeS 4850prime04primeprimeW)Serra dos Oacutergatildeos municipality ofCampina Grande do Sul

PR 1300ndash1630 Ribeiro Alves amp Haddad (2005)Clemente-Carvalho et al (2009)Clemente-Carvalho et al (2011b)Campos (2011)Fontoura Ribeiro amp Pie (2011)Pombal Jr amp Izecksohn (2011 including lsquolsquoPicoParanaacutersquorsquo) Firkowski (2013 without speciesidentification including lsquolsquoPico Paranaacutersquorsquo)Pie et al (2013)


pernix Getuacutelio (2514prime18primeprimeS 4850prime13primeprimeW) Serrados Oacutergatildeos municipality of CampinaGrande do Sul

PR 1450ndash1490 This study Pie et al (2013)


pernix Matildee Catira (2520prime51primeprimeS 4854prime25primeprimeW)Serra da Graciosa municipality of Qua-tro Barras

PR 1135ndash1405 Firkowski (2013 without species identification)Pie et al (2013 as lsquolsquoBrachycephalus sp nov 2rsquorsquo)


pernix Tupipiaacute (2514prime31primeprimeS 4847prime47primeprimeW) Serrados Oacutergatildeos municipality of Antonina

PR 1260 Firkowski (2013 without species identification)Pie et al (2013)

B ferruginus Southern Serrado Mar

pernix Olimpo (2527prime03primeprimeS 4854prime59primeprimeW) Serrado Marumbi municipality of Morretes

PR 965ndash1470 Alves et al (2006)Clemente-Carvalho et al (2009)Clemente-Carvalho et al (2011b)Pombal Jr amp Izecksohn (2011) Firkowski (2013without species identification) Pie et al (2013)

B fuscolinea-tus

Leste Catari-nense

pernix Morro do Bauacute (2647prime58primeprimeS4855prime47primeprimeW) municipality of Ilhota

SC 640ndash790 Firkowski (2013 without species identification)Pie et al (2013 as lsquolsquoBrachycephalus sp nov 9rsquorsquo)Ribeiro et al (2015)

B izecksohni Southern Serrado Mar

pernix Torre da Prata Serra da Prata(2537prime25primeprimeS 4841prime31primeprimeW) boundaryof the municipalities of MorretesParanaguaacute and Guaratuba

PR 980ndash1340 Ribeiro Alves amp Haddad (2005)Clemente-Carvalho et al (2009)Clemente-Carvalho et al (2011b)Pombal Jr amp Izecksohn (2011) Firkowski (2013without species identification) Pie et al (2013)

B leopardus Southern Serrado Mar

pernix Morro dos Perdidos (2553prime22primeprimeS4857prime22primeprimeW) municipality of Guaratuba



pernix Serra do Aracatuba (2554prime07primeprimeS4859prime47primeprimeW) municipality of Tijucas doSul

PR 1640 Firkowski (2013 without species identification)Pie et al (2013 as lsquolsquoBrachycephalus sp nov 4rsquorsquo)Ribeiro et al (2015)

B

mariaeterezaeSouthern Serrado Mar

pernix Reserva Particular do Patrimocircnio Natu-ral Caetezal top of the Serra Queimada(2606prime51primeprimeS 4903prime45primeprimeW) municipalityof Joinville



Bornschein

etal(2016)PeerJDO

I107717peerj24901541

Table 1 (continued)


B olivaceus Southern Serrado Mar

pernix Castelo dos Bugres (second position2613prime59primeprimeS 4903prime13primeprimeW) municipalityof Joinville



pernix Base of the Serra Queimada (2604prime57primeprimeS4903prime59primeprimeW) municipality of Joinville

SC 985 Pie et al (2013 as lsquolsquoBrachycephalus sp nov 7rsquorsquo)Ribeiro et al (2015)

B olivaceus Leste Catari-nense

Pernix Morro do Boi (2624prime42primeprimeS 4912prime59primeprimeW)municipality of Corupaacute

SC 690ndash920 This study MHNCI Pie et al (2013 aslsquolsquoBrachycephalus sp 3rsquorsquo)

B pernix Southern Serrado Mar

pernix Anhangava (2523prime19primeprimeS 4900prime15primeprimeW)Serra da Baitaca municipality of QuatroBarras

PR 1135ndash1405 Pombal Jr Wistuba amp Bornschein (1998)Wistuba (1998) Pires Jr et al (2005)Silva Campos amp Sebben (2007)Clemente-Carvalho et al (2009)Clemente-Carvalho et al (2011b)Campos Silva amp Sebben (2010) Campos (2011)Pombal Jr amp Izecksohn (2011) Firkowski (2013without species identification) Pie et al (2013)Ribeiro et al (2014)

B pombali Southern Serrado Mar

pernix Morro dos Padres (2536rsquo40primeprimeS4851prime22primeprimeW) Serra da Igrejamunicipality of Morretes

PR 1060ndash1300 Alves et al (2006) Clemente-Carvalho et al(2009) Clemente-Carvalho et al (2011b)Firkowski (2013 without species identification)Pie et al (2013)


pernix Trail to Morro dos Padres (2535prime58primeprimeS4851prime57primeprimeW) municipality of Morretes

PR 845ndash1060 Pie et al (2013)

B quiririensis Southern Serrado Mar

pernix Serra do Quiriri (2601prime17primeprimeS4859prime47primeprimeW) municipality of CampoAlegre

SC 1240ndash1318 Firkowski (2013 without species identification)Pie et al (2013 as lsquolsquoBrachycephalus sp nov 5rsquorsquo)Pie amp Ribeiro (2015)


pernix Serra do Quiriri (2601prime42primeprimeS4857prime11primeprimeW) municipality of Garuva

SC 1320ndash1380 Pie et al (2013 as lsquolsquoBrachycephalus sp nov 5rsquorsquo)Pie amp Ribeiro (2015)

B tridactylus Southern Serrado Mar

pernix Serra do Morato (2508prime09primeprimeS4817prime59primeprimeW) Reserva Natural SaltoMorato municipality of Guaraquecaba

PR 805ndash910 This study DZUP Garey et al (2012)Bornschein et al (2015)

B verrucosus Southern Serrado Mar

pernix Morro da Tromba (2612prime44primeprimeS4857prime29primeprimeW) municipality of Joinville


Brachycephalussp 4


pernix Morro do Canal (2530prime55primeprimeS4858prime56primeprimeW) municipality of Piraquara

PR 1320 DZUP Firkowski (2013 without speciesidentification)

Brachycephalussp 4


pernix Morro do Vigia (2530prime33primeprimeS4858prime58primeprimeW) municipality of Piraquara


Brachycephalussp 5


pernix Pedra Branca do Araraquara (2556prime00primeprimeS4852prime50primeprimeW) Serra do Araraquara mu-nicipality of Guaratuba



Bornschein

etal(2016)PeerJDO

I107717peerj24901641

Table 1 (continued)


Brachycephalussp 5


pernix Serra Canasvieiras (2536prime58primeprimeS4846primeprime59primeprimeW) boundary of themunicipalities of Guaratuba andMorretes

PR 1080 This study DZUP Firkowski (2013 withoutspecies identification)

Brachycephalussp 6


pernix Serra do Salto (2542prime07primeprimeS 4903prime44primeprimeW)Malhada District municipality of SatildeoJoseacute dos Pinhais

PR 1095ndash1160 This study DZUP Firkowski (2013 withoutspecies identification) Pie et al (2013as lsquolsquoBrachycephalus sp 2rsquorsquo)

Excluded recordsf


didactylus Ubatuba SP Silva Campos amp Sebben (2007)Campos Silva amp Sebben (2010) Campos (2011)

B hermogenesi Paranapiacaba didactylus Municipality of Piedade SP Condez Sawaya amp Dixo (2009)Clemente-Carvalho et al (2011b)


ephippium Santa Teresa ES Pombal Jr amp Gasparini (2006)Pombal Jr amp Izecksohn (2011)

B cf crispus Central Serrado Mar

ephippium Cunha SP Campos Silva amp Sebben (2010 aslsquolsquoBrachycephalus sp 3rsquorsquo) Campos(2011 as lsquolsquoBCU SP2rsquorsquo)


ephippium Atibaia SP Pires Jr et al (2003) Pires Jr et al (2005)Ananias Giaretta amp Recco-Pimentel (2006)Clemente-Carvalho et al (2008)Clemente-Carvalho et al (2009)Clemente-Carvalho et al (2011b)Clemente-Carvalho et al (2011a)Clemente-Carvalho et al (2016)Campos Silva amp Sebben (2010) Campos (2011as lsquolsquoBAT SP3rsquorsquo) Pombal Jr amp Izecksohn (2011)


ephippium Itamonte MG Silva Campos amp Sebben (2007)Campos Silva amp Sebben (2010) Campos (2011as lsquolsquoBIT MG1rsquorsquo)


ephippium Itatiaia RJ Pombal Jr amp Izecksohn (2011)


ephippium Joaquim Egiacutedio SP Clemente-Carvalho et al (2016)


ephippium Jundiaiacute SP Miranda-Ribeiro (1920)Clemente-Carvalho et al (2008)Clemente-Carvalho et al (2011a)


ephippium Piquete SP Miranda-Ribeiro (1920)Pombal Jr amp Izecksohn (2011)


Bornschein

etal(2016)PeerJDO

I107717peerj24901741

Table 1 (continued)



ephippium Angra dos Reis RJ Pombal Jr amp Izecksohn (2011)


ephippium Floresta da Tijuca municipality of Rio deJaneiro

RJ Pombal Jr amp Izecksohn (2011)


ephippium Guapiacu (2226prime34primeprimeS 4245prime38primeprimeW)municipality of Cachoeira de Macacu



ephippium Mangaratiba RJ Campos (2011 as lsquolsquoBMA RJ1rsquorsquo)Pombal Jr amp Izecksohn (2011)


ephippium Parque Nacional da Serra dos Oacutergatildeos RJ Pombal Jr amp Izecksohn (2011)


ephippium Rio de Janeiro RJ Pombal Jr amp Izecksohn (2011)


ephippium Teresoacutepolis RJ Pires Jr et al (2002) Pires Jr et al (2005)Silva Campos amp Sebben (2007)Campos Silva amp Sebben (2010) Campos (2011as lsquolsquoBTE RJ4rsquorsquo) Pombal Jr amp Izecksohn (2011)


ephippium Bocaina SP Pombal Jr amp Izecksohn (2011)


ephippium Cotia SP Silva Campos amp Sebben (2007)Campos Silva amp Sebben (2010)Campos (2011 as lsquolsquoBCO SP5rsquorsquo)


ephippium Fazenda Papagaio Serra da Bocaina SP Pombal Jr amp Izecksohn (2011)


ephippium Mogi das Cruzes SP Pires Jr et al (2005) Silva Campos amp Sebben(2007) Campos Silva amp Sebben (2010)Campos (2011 as lsquolsquoBMC SP4rsquorsquo)Pombal Jr amp Izecksohn (2011)


ephippium Serra da Bocaina SPRJ Pombal Jr amp Izecksohn (2011)


ephippium Nova Friburgo RJ Silva Campos amp Sebben (2007 aslsquolsquoB ephippiumrsquorsquo) Campos Silva amp Sebben(2010 as lsquolsquoB ephippiumrsquorsquo) Campos (2011)

B margarita-tus


ephippium Siacutetio do Pau Ferro Morro Azul munici-pality of Engenheiro Paulo de Frontin


B cfmargari-tatus


ephippium Petroacutepolis RJ Campos (2011 as lsquolsquoBPT RJ3rsquorsquo)


ephippium Salesoacutepolis SP Pires Jr et al (2005)


ephippium Santana de Parnaiacuteba SP Abegg et al (2015)


Bornschein

etal(2016)PeerJDO

I107717peerj24901841

Table 1 (continued)



ephippium Ubatuba SP Silva Campos amp Sebben (2007as lsquolsquoBrachycephalus cf vertebralisrsquorsquo)Campos Silva amp Sebben (2010 aslsquolsquoBrachycephalus cf vertebralisrsquorsquo) Campos (2011)


ephippium Cunha SP Pombal Jr (2001)


ephippium Parati RJ Silva Campos amp Sebben (2007)Campos Silva amp Sebben (2010) Campos (2011)

Brachycephalussp 7

Central Serrado Mar

ephippium Biritiba-Mirim SP Silva Campos amp Sebben (2007 aslsquolsquoB nodotergarsquorsquo) Campos Silva amp Sebben (2010as lsquolsquoBrachycephalus sp 1rsquorsquo)Campos (2011 as lsquolsquoBBM SP1rsquorsquo)


pernix Campina Grande do Sul PR Silva Campos amp Sebben (2007)Campos Silva amp Sebben (2010) Campos (2011)

Brachycephalusleopardus


pernix Tijucas do Sul PR Campos (2011 as lsquolsquoBTS PRrsquorsquo)

B atelopoides SouthernSerra da Man-tiqueira

Piquete SP Miranda-Ribeiro (1920)

Brachycephalussp cf Brachy-cephalussp 1

Paranapiacaba didactylus Municipality of Ribeiratildeo Grande SP Verdade et al (2008 as lsquolsquoB hermogenesirsquorsquo)


Paranapiacaba didactylus Municipality of Tapiraiacute SP Verdade et al (2008 as lsquolsquoB hermogenesirsquorsquo)Condez Sawaya amp Dixo (2009as lsquolsquoB hermogenesirsquorsquo)


Paranapiacaba didactylus Municipality of Juquitiba SP Verdade et al (2008 as lsquolsquoB hermogenesirsquorsquo)


Central Serrado Mar

didactylus Estacatildeo Ecoloacutegica Jureacuteia-Itatins munici-pality of Iguape

SP Verdade et al (2008 as lsquolsquoB hermogenesirsquorsquo)


Bornschein

etal(2016)PeerJDO

I107717peerj24901941

Table 1 (continued)




didactylus Ilha do Cardoso municipality ofCananeacuteia

SP Verdade et al (2008 as lsquolsquopossibly B

hermogenesirsquorsquo)

NotesaSpecies and records are ordered by the following criteria alphabetic order of groups and alphabetic order of species by groupsbAccording to IBAMA (2007) with additional subdivisions (see lsquoMaterials and Methodsrsquo)cFor group definitions see lsquoMaterials and MethodsrsquodGeographical coordinates are based on the datumWGS84eDZUP Colecatildeo de Herpetologia Departamento de Zoologia Universidade Federal do Paranaacute state of Paranaacute Brazil MHNCI Museu de Histoacuteria Natural Capatildeo da Imbuia Prefeitura Municipal de Cu-ritiba state of Paranaacute BrazilfExcluded records represent vague localities general reference of municipality of locality and localities that were specified but could not be located or were questionable given exceedingly low associatedaltitude

Bornschein

etal(2016)PeerJDO

I107717peerj24902041

Table 2 Number of species of Brachycephalus per relief unit

Relief unita Number of groups Number of species (undescribedspecies included)

Preacute-Litoracircneas 1 1 (0)Serra da Mantiqueira 2 3 (0)

Northern Serra da Mantiqueira 2 3 (0)Southern Serra da Mantiqueira 1 1 (0)

Paraiacuteba do Sul 1 1 (0)Serra do Mar 3 30 (6)

Northern Serra do Mar 2 6 (1)Central Serra do Mar 2 9 (1)Southern Serra do Mar 2 16 (4)

Paranapiacaba 1 1 (1)Leste Catarinense 1 3 (0)

NotesaAccording to IBAMA (2007) with additional subdivisions in the units Serra da Mantiqueira and Serra do Mar (see lsquoMaterialsand Methodsrsquo)

A third undescribed species was assigned to the didactylus group because it representsa population to be split from B hermogenesi (Pie et al 2013) a representative speciesfrom the didactylus group Finally the other three populations were assigned to the pernixgroup because they were previously assigned to the lsquolsquopernix cladersquorsquo (Pie et al 2013) whosemembers all belong to the pernix group (Ribeiro et al 2015)

RESULTSThe final dataset is composed of 333 records (from73 distinc sources) of 120 localities (threeof which representing novel unpublished records) These records involve the geographicoccurrence of 28 formally known and six undescribed species including 82 previousrecords that had been excluded based on the accuracy criteria indicated above (Table 1)Species were recorded in six relief units the richest of them being Serra do Mar with 30species (six undescribed Fig 1) followed by Serra da Mantiqueira and Leste Catarinensewith three species each (Table 2) Northern Serra da Mantiqueira has records of all threespecies of this relief unit while Southern Serra da Mantiqueira has records of only onespecies In Serra do Mar species richness increases from north to south with records of sixspecies (one undescribed) in Northern Serra do Mar nine (one undescribed) in CentralSerra do Mar and 16 (four undescribed) in Southern Serra do Mar (Table 2 Fig 1)Finally Preacute-Litoracircneas Paraiacuteba do Sul and Paranapiacaba relief units have records ofonly one species each (Paranapiacaba has records of an undescribed species Table 2) Thenorthernmost and southernmost records are 1592 km distant from each other in a straightline the species recorded in these limits are B pulex and B fuscolineatus respectively(Table 1)

The didactylus group comprises four species (one undescribed) encompassing thebroadest geographical distribution of all three groups from the northernmost record forthe genus (state of Bahia with B pulex) southward to the north of Santa Catarina state


Figure 1 Geographical and altitudinal distribution of Brachycephalus spp according to their respec-tive species group (light gray= didactylus black= ephippium and dark gray= pernix group) acrossthe three sectors of the Serra doMar relief unit The species connections represent the occurrence ineach sector of the relief unit and in altitudinal quotas The width of the connections (in both directions)represents the proportional amount of citations in the bibliography for each sector and altitude quotas(wider=more citations) See Table 4 for the correspondence of the acronyms with the species name


Figure 2 Occurrence records of Brachycephalus spp (A) all species (B) species of the didactylus group(C) species of the ephippium group (D) species of the pernix group Diamonds records of the ephip-pium group circles records of the didactylus group and squares records of the pernix group Abbrevia-tions BA Bahia MG Minas Gerais ES Espiacuterito Santo RJ Rio de Janeiro SP Satildeo Paulo PR Paranaacute andSC Santa Catarina Relief units modified from IBAMA (2007)

with Brachycephalus sp 1 (Table 1 Fig 2B) Three species occur in Serra do Mar (oneundescribed) but only one species occurs in each of Northern Central and Southern Serrado Mar (Southern Serra do Mar has records of one undescribed species Table 3) Onlyone species occurs in the three remaining relief units with presence of this group (Preacute-Litoracircneas Serra da Mantiqueira and Paranapiacaba with the latter being represented byan undescribed species Table 3) There are no records of this group inland in the lsquolsquoSouthernSerra da Mantiqueirarsquorsquo but there are records relatively further inland in lsquolsquoParanapiacabarsquorsquoin the state of Paranaacute (Fig 2B)

The ephippium group comprises 13 species (two undescribed Table 1) It has a moreintermediate geographical distribution in relation to the overall latitudinal distributionof the genus from the state of Espiacuterito Santo to southern state of Satildeo Paulo (Fig 2C)


Table 3 Number of species of Brachycephalus per group in each relief unit

Relief unita Number of species per group (undescribed species included)

didactylus ephippium pernix

Preacute-Litoracircneas 1 (0) 0 0Serra da Mantiqueira 1 (0) 2 (0) 0

Northern Serra da Mantiqueira 1 (0) 2 (0) 0Southern Serra da Mantiqueira 0 1 (0) 0

Paraiacuteba do Sul 0 1 (0) 0Serra do Mar 3 (1) 12 (2) 15 (3)

Northern Serra do Mar 1 (0) 5 (1) 0Central Serra do Mar 1 (0) 8 (1) 0Southern Serra do Mar 1 (1) 0 15 (3)

Paranapiacaba 1 (1) 0 0Leste Catarinense 0 0 3 (0)

NotesaAccording to IBAMA (2007) with additional subdivisions in the units Serra da Mantiqueira and Serra do Mar (see Materialsand methods)

the species recorded in those extreme geographical limits are B alipioi and B ephippiumrespectively The group is represented in all relief units encompassed in this region (SerradaMantiqueira Paraiacuteba do Sul and Serra doMar Table 1 Fig 2C) It is highly representedby species in Serra do Mar (12 species two of which undescribed Fig 1) whereas in Serrada Mantiqueira there is records of two species and in Paraiacuteba do Sul of only one (Table 3)Northern Serra da Mantiqueira has two species while Southern Serra da Mantiqueira hasonly one (Table 3) Northern Serra do Mar has five species (one undescribed) and CentralSerra do Mar has eight species (also with one undescribed) Southern Serra do Mar doesnot harbor any species of this group (Table 3 Fig 1)

The pernix group is the most species-rich group with 17 species (three undescribedTable 1) It has the smallest geographical distribution restricted to the states of Paranaacuteand Santa Catarina southern Brazil (Fig 1) comprising the southernmost distribution ofthe genus with B fuscolineatus being recorded 87 km south of the border of the state ofParanaacute the northernmost species is B tridactylus (Table 1) Per relief unit 15 species (threeundescribed) occurs in Southern Serra do Mar and three in Leste Catarinense (Table 3Fig 1)

We were able to determine the extent of occurrence of 17 species (515 of all specieswith records at precise locations Table 4) Two species of the didactylus group have thehighest estimated extent of occurrence with over 500 thousand ha namely Brachycephalussp 1 and B hermogenesi On the other hand estimates of extents of occurrence for allremaining species did not reach 20 thousand haWith proportionally intermediate extent ofoccurrence there are tree species from the ephippium group (B garbeanus B margaritatusand B pitanga) with estimates between 2ndash19 thousand ha and five species from the pernixgroup (B olivaceus B brunneus B ferruginus Brachycephalus sp 6 and B quiririensis)with estimates between 1ndash6 thousand ha (Table 4) There are four species with small extent


Figure 3 Species richness of Brachycephalus in each altitudinal class (including undescribed species)(A) all species (B) species of the didactylus group (C) species of the ephippium group (D) species of thepernix group

of occurrence between 100ndash500 hectares one from the didactylus groupmdashB pulexmdashandthree from the pernix groupmdashB pernix B izecksohni and B leopardus (Table 4) Finallythere are three species from the pernix group with highly reduced extents of occurrencenamely B tridactylus B fuscolineatus and B boticario with 4142 ha 2363 ha and 1107ha respectively (Table 4)

Brachycephalus species are found from sea level to at least 1900 m asl (Tables 1 and 3)The ephippium group was characterized by species with the broadest altitudinal amplitude(1700 m Table 4) The didactylus and pernix groups had similar altitudinal amplitude(1110 m and 1185 m respectively Table 4) However the altitudinal occurrence of thedidactylus group started at sea level whereas the pernix group began at mid-elevations (455m asl Table 4)

The altitudinal class with the highest species richness was 751ndash1000 m asl with 21species (three undescribed Fig 3A) The highest species richness for the didactylus groupwas also found between 751ndash1000 m asl including all four species of the group (oneundescribed Fig 3B) The highest richness of the ephippium group was evenly recordedbetween 751ndash1000 m comprising eight species (one undescribed Fig 3C) Finally mostspecies of the pernix group were found between 1001ndash1250 m asl totalizing 10 species(three undescribed Fig 3D)

The species with the broadest altitudinal range was B didactylus (1075 m starting at 35m asl) and Brachycephalus sp 1 (1035 m starting at 25 m asl) both included in thedidactylus group and B ephippium (1050 m starting from 200 m asl) included in theephippium group (Table 4) The largest altitudinal occurrence amplitude for species of thepernix group was recorded in B brunneus (535 m starting at 1095 m asl Table 4) Thelowest records for the pernix group were at 845 m asl in the state of Paranaacute and at 455 masl in the state of Santa Catarina southern Brazil (Table 1) This illustrates the tendency


Table 4 Altitudinal distribution and lsquolsquoextent of occurrencersquorsquo (sensu IUCN 2012) of Brachycephalusspp Only confirmed altitudinal records are considered Extent of occurrence by altitude (Alt) or by anadaptation of the minimum convex polygon (MCP see text for details)

Speciesa Altitudinal distribution (m asl) Extent of occurrence (ha)

Range Amplitude Alt MCP

didactylus group 0ndash1110 1110 ndash ndashB didactylus (dida) 35ndash1110 1075 B hermogenesi (herm) 0ndash900 900 ndash 56758987B pulex 800ndash930 130 48825 ndashBrachycephalus sp 1 (sp1) 25ndash1060 1035 ndash 77845842ephippium group 200ndash1900 1700 ndash ndashB alipioi 1070ndash1100 30 B crispus (cris) 800ndash1100 300 B ephippium (ephi) 200ndash1250 1050 B garbeanus (garb) 1130ndash1900 770 ndash 1226800B guarani (guar) 500ndash900 400 B margaritatus (marg) 600ndash980 380 ndash 1827287B nodoterga (nodo) 700ndash945 245 B pitanga (pita) 900ndash1140 240 ndash 237707B toby (toby) 750 0 B vertebralis (vert) 900 0 Brachycephalus sp 2 (sp2) 1100ndash1200 100 Brachycephalus sp 3 (sp3) 800ndash825 25 pernix group 455ndash1640 1185 ndash ndashB auroguttatus (auro) 1070ndash1100 30 B boticario 755ndash795 40 1107 ndashB brunneus (brun) 1095ndash1630 535 568708 ndashB ferruginus (ferr) 965ndash1470 505 547551 ndashB fuscolineatus 640ndash790 150 2363 ndashB izecksohni (izec) 980ndash1340 360 35043 ndashB leopardus (leop) 1400ndash1640 240 17673 ndashB mariaeterezae (mari) 1265ndash1270 5 B olivaceus (oliv) 690ndash985 295 ndash 1253164B pernix (pern) 1135ndash1405 270 43210 ndashB pombali (pomb) 845ndash1300 455 B quiririensis (quir) 1240ndash1380 140 133897 ndashB tridactylus (trid) 805ndash910 105 4142 ndashB verrucosus (verr) 455ndash945 490 Brachycephalus sp 4 (sp4) 1250ndash1320 70 Brachycephalus sp 5 (sp5) 1000ndash1080 80 Brachycephalus sp 6 (sp6) 1095ndash1160 65 221154 ndash

NotesaAbreviation in parentheses refers to species acronyms in Fig 1


Figure 4 Altitudinal amplitude records of Brachycephalus spp from the pernix group binned into lati-tudinal classes (including undescribed species) Diamonds indicate median values

for the altitudinal distribution of species of the pernix group to decrease with increasinglatitude (Fig 4)

Syntopy inBrachycephalus is rare being reported for the didactylus and ephippium groupsin state of Rio de Janeiro and Satildeo Paulo and for the didactylus and pernix groups in the stateof Paranaacute and Santa Catarina (Table 1) Between didactylus and ephippium groups syntopyhas been reported in four localities between B didactylus and B ephippium in the ReservaEcoloacutegica Rio das Pedras Rio de Janeiro (Carvalho-e-Silva Silva amp Carvalho-e-Silva 2008Almeida-Santos et al 2011 Rocha et al 2013) between B didactylus and B margaritatusin the Sacra Famiacutelia do Tinguaacute Rio de Janeiro (Izecksohn 1971 Pombal Jr 2001 Ribeiroet al 2005 Alves et al 2006 Alves et al 2009 Silva Campos amp Sebben 2007 Verdade etal 2008 Clemente-Carvalho et al 2009 Campos 2011 Pombal Jr amp Izecksohn 2011 Pieet al 2013) between B didactylus and Brachycephalus sp 2 in Theodoro de OliveiraRio de Janeiro (Siqueira et al 2011 Siqueira Vrcibradic amp Rocha 2013) and between Bhermogenesi and B ephippium in the Reserva Florestal de Morro Grande Satildeo Paulo (Dixoamp Verdade 2006 Verdade et al 2008) Between didactylus and pernix groups two cases ofsyntopy have been recorded (M Bornschein pers obs 2016) one between Brachycephalussp 1 (didactylus group) and B tridactylus in Reserva Particular do Patrimocircnio NaturalSalto Morato at 900 m asl and the another one between Brachycephalus sp 1 and Bolivaceus at Castelo dos Bugres between 800ndash835 m asl (M Bornschein pers obs 2011Table 1)

Sympatry and possibly syntopy also between didactylus and ephippium groups wasreported in the state of Satildeo Paulo in two localities (Table 1) between B hermogenesi andBrachycephalus sp 3 in the Reserva Bioloacutegica do Alto da Serra de Paranapiacaba (Verdadeet al 2008 Pie et al 2013) and between B hermogenesi and B nodoterga in the Estacatildeo


Bioloacutegica de Boraceacuteia (Pombal Jr Wistuba amp Bornschein 1998 Pombal Jr 2001 PombalJr 2010 Ribeiro et al 2005 Alves et al 2006 Alves et al 2009 Pimenta Beacuternils amp PombalJr 2007 Verdade et al 2008 Haddad et al 2010 Pombal Jr amp Izecksohn 2011 Pie et al2013) A sympatry may occur between species of a single group particularly the ephippiumgroup in the state of Rio de Janeiro (Table 1) between B bufonoides and B garbeanusin the Serra de Macaeacute (Miranda-Ribeiro 1920 Pombal Jr 2010 Pombal Jr amp Izecksohn2011) and between B ephippium and B vertebralis in the Pedra Branca municipalityof Parati (Pombal Jr 2001 Pombal Jr 2010 Clemente-Carvalho et al 2009 PombalJr amp Izecksohn 2011 Pie et al 2013) Both need confirmation (see Pombal Jr 2001)

DISCUSSIONThe northernmost and southernmost relief units are poorly represented by records ofBrachycephalus namely Preacute-Litoracircneas and Leste Catarinense respectively This suggeststhe possibility that the genus occurs farther north and south from the most extremerecords known today (see Fig 2) Interestingly the potential distribution of Brachycephalusthrough environmental niche modeling (Pie et al 2013) is consistent with the possibilityof a wider distribution of the genus to the south of the current distribution spreadingwidely through the Leste Catarinense relief unit (see Figs 3A 3B 3E 3F and 4A of Pie et al(2013)) Forests at lower altitudes in the Preacute-Litoracircneas region are different from those inmountains at higher altitudes displaying for example little moss on tree trunks and scarceepiphytic plants (MRB amp RB-L per obs) We believe it is possible that the occurrenceof the genus in this relief unit is restricted to mountains Examples of locations of scarcehumid mountains of this region can be seen in Mauriacutecio et al (2014) who mapped theoccurrence of an endemic mountain bird to the Preacute-Litoracircneas relief unit the Scytalopusgonzagai The environmental niche modeling of Brachycephalus indeed indicates a smallarea of suitable habitats in this region (see Fig 3B of Pie et al 2013)

The occurrence of B ephippium in distinct relief units should be the subject of furtherscrutiny In particular populations under that name might indeed represent crypticspecies that would have to be split (see also Dixo amp Verdade 2006 Silva Campos amp Sebben2007 Clemente-Carvalho et al 2008 Clemente-Carvalho et al 2011a Campos Silva ampSebben 2010 Campos 2011 Siqueira Vrcibradic amp Rocha 2013 Trevine et al 2014)Similar conditions were detected in a montane bird Scytalopus speluncae (taxonomyaccording to Mauriacutecio et al (2010)) which has to be split into several new species Infact the distribution of S speluncae is congruent with that of B ephippium in some reliefunits (Mata et al 2009) The occurrence of B ephippium around the city of Satildeo Paulois of particular interest given this region is characterized as a contact between Serra daMantiqueira and Serra do Mar relief units (IBGE 1993)

For a long time all known species of Brachycephalus of the pernix group had theirgeographical distribution limited to a single lsquolsquoSerrarsquorsquo ie in a massif range with highaltitudes isolated from other lsquolsquoSerrasrsquorsquo by areas of lower altitudes Pie et al (2013) werethe first to report the occurrence of more than one species of the pernix group in a singlelsquolsquoSerrarsquorsquo and here we report on other similar situations In addition the present study is


the first to report the occurrence of a species of this group distributed in two lsquolsquoSerrasrsquorsquoThis is the case of B brunneus distributed in Serra dos Oacutergatildeos (not to be confused withthe homonym lsquolsquoSerrarsquorsquo of the state of Rio de Janeiro) and Serra da Graciosa (Table 1)Distributions of more than one species in a single lsquolsquoSerrarsquorsquo involve the cases of B ferruginusandBrachycephalus sp 4 distributed in Serra doMarumbi andB leopardusB auroguttatusand B quiririensis distributed in Serra do AracatubaSerra do Quiriri a single mountainmassif in the border of the states of Paranaacute and Santa Catarina (Table 1) These cases donot represent syntopy because all of them are isolated from each other by more than 3 kmThe ocurrences of two species of the ephippium group in a single Serra are known for longtime ie 1920 (involving B bufonoides and B garbeanus Miranda-Ribeiro (1920)) and2001 (involving B ephippium and B vertebralis Pombal Jr (2001))

It is interesting to note that the species with low altitudinal records (and also with highaltitudinal amplitude of occurrence) are the ones of greatest extent of occurrencemeasuredperhaps indicating that its relatively plastic condition provide them a major opportunityto establish through a continuous Atlantic Forest In the other way species with mediumto high lower limit of altitudinal occurrence and also with moderate altitudinal amplitudeof occurrence have very reduced extent of occurrence indicating proportionaly reducedplasticity and subjection of environmental and topographic constrains In a study ona Neotropical bird Reinert Bornschein amp Firkowski (2007) showed that a very detailedestimate of the species extent of occurrence resulted in an area seven times greater than thearea of occupancy which underscores howmuch the extent of occurrence ofBrachycephaluscould be overstimated In comparison the small extent of occurrence of the Brachycephalusis not the smaller lsquolsquorangersquorsquo of species in the world among the smaller there are an isopodand a fish with less than 001 ha of occurrence each (Brown Stevens amp Kaufman 1996)However they are between the smallest lsquolsquorangesrsquorsquo of vascular plants and fishes of the world(lt100 ha) and much smaller than the smallest lsquolsquorangesrsquorsquo of birds and mammals of the world(sim1000000 ha Brown Stevens amp Kaufman (1996))

The altitudinal records indicate that the pernix and ephippium groups are indeedlsquolsquomontane groupsrsquorsquo (Figs 1 and 3) even though the altitudinal amplitude of species of theephippium groupmight be underestimatedOccasional records below 500masl for speciesof both montane groups do not mean that all lsquolsquomontane speciesrsquorsquo of the genus normallyoccur at lower altitudes with the absence of lower records resulting from sampling biasRather one could expect that species of the pernix group at higher latitudes would tendto be recorded at lower altitudes due to climatic compensation Moreover local recordsat lower altitudes of species of montane groups can be due to particular local conditionsof high moisture resulting from peculiar topographical features Regardless of the extremealtitudinal records each species must have an altitudinal range that corresponds to itsclimatic optimum (see Fig 1) Studies estimating abundance along altitudinal transects canbe used not only to determine altitudinal ranges but also the climatic optimum for eachspecies These data are of particular interest in the context of long-term studies to assessthe impact of climatic changes with gradual modification in the abundances and evenchanges in the altitudinal range being expected over time (see Corn 2005 Jump Huang ampChou 2012)


All records of pernix group species in the state of Paranaacute were eithermade in cloud forests(lsquolsquoFloresta Ombroacutefila Densa Alto-montanarsquorsquo sensu Veloso Rangel-Filho amp Lima (1991)) orin the transition zones between cloud forest and montane forests (lsquolsquoFloresta OmbroacutefilaDensa Montanarsquorsquo) The only exception is B tridactylus which occurs in montane forests(this study since there is no available description for the forest type in the species descriptionby Garey et al 2012) Cloud or elfin forests are pygmy tropical forests that occur in highlyhumid regions at the cloud level between 1000 to 2500 m asl (Walter 1977) In thestate of Paranaacute these forests occur from 900 m to about 1850 m asl (Struminski 1997Bornschein et al 2012) The lowest record of B pombali (845 m asl) in the transitionbetween cloud forest and montane forest probably represents the lowest altitude of thistransition in the state of Paranaacute In Santa Catarina species from the pernix group occurin cloud forests montane forests and in the transition between them The only knownexception of forest habitat in the pernix group involves the observation of B izecksohnialso in herbaceous montane fields (lsquolsquocampos de altitudersquorsquo or lsquolsquorefuacutegio vegetacionalrsquorsquo sensuVeloso Rangel-Filho amp Lima (1991) M Bornschein pers obs 2000)

The few cases of syntopy between species not only show little altitudinal overlap butalso involve species of different groups consistent with the notion that closely relatedspecies remain allopatric Localities with sympatry and syntopy are particularly interestingfor further studies related to the altitudinal distribution of species On the other handsympatry between species of the groups ephippium and pernix is not expected given that agap of 208 km occurs between species of these groups It is interesting to note that only themontane species groups ie ephippium and pernix are highly species-rich yet they tendnot to show sympatry (although there are some species distributed very close to each otherand that there are cases of distinct species occurring in a single lsquolsquoSerrarsquorsquo) We believe thatthese conditions suggest that these groups evolved in allopatry andor parapatry while theAtlantic Forest experienced retraction and isolation as islands between grasslands Duringthe Quaternary climatic conditions changed cyclically from cold and dry to warmer andwet periods and these shifts were responsible for the cyclical retraction and expansionof forest coverage respectively (eg Behling amp Lichte 1997 Behling et al 2002 BehlingPillar amp Depatta 2005 Behling et al 2007 Behling 2007 Langone et al 2008 Behling ampSafford 2010 Enters et al 2010 Hessler et al 2010) In colder climates montane forestsmay have dispersed to lower altitudes allowing species of Brachycephalus to disperse Insubsequent warmer and wet climate the montane forest may have dispersed to higheraltitudes isolating populations of Brachycephalus and favoring speciation

In relation to the species distributed close to each other or in single lsquolsquoSerrasrsquorsquo withoutapparent geographic barriers it is possible that the expansion and retraction of forestsdid not occur homogeneously across altitudinal quotas but it might have occurred asisolated patches even in restricted areas In areas where climatic conditions favored thereturn of a vast forest cover geographically close species would have lost the correspondingenvironmental barriers remaining allopatric probably due to ecological requirements Themost notable case of proximity between species occurs in northeastern state of Satildeo Paulowhere higher mountains are absent and five species occur in a single plateau (B crispus


B guarani B pitanga B toby and B vertebralis) In this region the forests may have beenconfined in valleys during the periods of retraction in the forest distribution

In conclusion Brachycephalus is restricted to the eastern portion of the Atlantic Forestbiome with species occurring in allopatry or at least in parapatry with rare cases ofsyntopy The species of the genus are segregated in three groups of species with oneof them (didactylus) including species that respond differently to altitude occurring inlower altitudes and having greater geographic distributions being much more ecologicalytolerant and plastic Species from the remaining groups (ephippium and pernix) depend onhigh altitude conditions and can be found locally in lower altitudes probably in responseto particular microclimatic conditions Sympatric species include members of distinctspecies groups and are in contact only in the altitudinal limits of each other (higher limitfor the lsquolsquolowlandrsquorsquo species and lower limit for the lsquolsquomontanersquorsquo species) Apart from a fewspecies most of them have restricted extents of occurrence to the point that many aremicroendemic occurring in mountain tops with a total extent of occurrence comparableto the smallest range from species around world The microhabitat requirements of thespecies can prevent more realistic estimatives of extent of occurrence with traditionalmethodologies possibly resulting in substantial bias This same feature makes the species ofparticular interest to monitor climate change through their abundances along altitudinalgradients The genus also can be used as a model to infer historical environmental changesdue to climatic changes given that speciation in Brachycephalus species is thought to haveresulted from vicariant processes following upward dispersal of montane forests throughaltitudinal ranges in past warm and wet climates

ACKNOWLEDGEMENTSWe thank Magno V Segalla and Camila R Alves for valuable assistance during fieldworkClaudia Golec helped in the compilation of bibliography Two anonymous refereesimproved the manuscript with valuable comments and suggestions

ADDITIONAL INFORMATION AND DECLARATIONS

FundingMRB received a PRODOC grant from CAPES (project 25992010) RBL is supportedby fellowships from CNPqMCT (1418232011ndash9) MRP is supported by grant fromCNPqMCT (5713342008ndash3) Fieldwork during 2011 and 2012 was partially funded byFundacatildeo Grupo O Boticaacuterio de Protecatildeo agrave Natureza (trough the project 0895_20111conducted by Mater NaturamdashInstituto de Estudos Ambientais) The funders had no rolein study design data collection and analysis decision to publish or preparation of themanuscript

Grant DisclosuresThe following grant information was disclosed by the authorsCAPES 25992010


CNPqMCT 1418232011ndash9 5713342008ndash3Fundacatildeo Grupo O Boticaacuterio de Protecatildeo agrave Natureza 0895_20111

Competing InterestsMarcio Pie is an Academic Editor for PeerJ Seacutergio AA Morato is employed by STCPEngenharia de Projetos Ltda

Author Contributionsbull Marcos R Bornschein conceived and designed the experiments performed theexperiments analyzed the data contributed reagentsmaterialsanalysis tools wrotethe paper prepared figures andor tables reviewed drafts of the paper compiled thedatabull Carina R Firkowski Leandro Correcirca Luiz F Ribeiro and Seacutergio AA Morato analyzedthe data reviewed drafts of the paperbull Ricardo Belmonte-Lopes and Andreas LS Meyer analyzed the data prepared figuresandor tables reviewed drafts of the paperbull Reuber L Antoniazzi-Jr analyzed the data prepared figures andor tablesbull Bianca L Reinert and Felipe A Cini analyzed the databull Marcio R Pie analyzed the data contributed reagentsmaterialsanalysis tools revieweddrafts of the paper

Field Study PermissionsThe following information was supplied relating to field study approvals (ie approvingbody and any reference numbers)

Collection and research permits for this study were issued by ICMBIO (22470ndash1 and22470ndash2) Instituto Ambiental do Paranaacute (permit 35511) and Fundacatildeo Municipal doMeio Ambiente of Joinville (permit 00111) for the regional permits

Data AvailabilityThe following information was supplied regarding data availability

The raw data in this article is included in the tables and figures

REFERENCESAbegg AD Ortiz FR Rocha B Condez TH 2015 A new record for Brachycephalus

nodoterga (Amphibia Anura Brachycephalidae) in the state of Satildeo Paulo BrazilCheck List 11Article 1769 DOI 10155601151769

Almeida FFM de Carneiro C dal R 1998 Origem e evolucatildeo da Serra do Mar RevistaBrasileira de Geociecircncias 28135ndash150

Almeida-Santos M Siqueira CC Van Sluys M Rocha CFD 2011 Ecology of theBrazilian flea frog Brachycephalus didactylus (Terrarana Brachycephalidae) Journalof Herpetology 45251ndash255 DOI 10167010-0151

Alves ACR Ribeiro LF Haddad CFB Reis SF dos 2006 Two new species of Brachy-cephalus (Anura Brachycephalidae) from the Atlantic Forest in Paranaacute Statesouthern Brazil Herpetologica 62221ndash233 DOI 10165505-411


Alves ACR Sawaya RJ Reis SF dos Haddad CFB 2009 New species of Brachycephalus(Anura Brachycephalidae) from the Atlantic Rain Forest in Satildeo Paulo State South-eastern Brazil Journal of Herpetology 43212ndash219 DOI 1016700022-1511-432212

Amaro RC Rodrigues MT Yonenaga-Yassuda Y Carnaval AC 2012 Demographicprocesses in the montane Atlantic rainforest molecular and cytogenetic evidencefrom the endemic frog Proceratophrys boieiMolecular Phylogenetics and Evolution62880ndash888 DOI 101016jympev201111004

Ananias F Giaretta AA Recco-Pimentel SM 2006 Cytogenetics of Brachycephalusephippium (Anura Brachycephalidae) with comments on its relationship to theBufonidae Amphibia-Reptilia 27121ndash125 DOI 101163156853806776052065

Arauacutejo CB de Guerra TJ Amatuzzi MCO Campos LA 2012 Advertisement andterritorial calls of Brachycephalus pitanga (Anura Brachycephalidae) Zootaxa330266ndash67

Behling H 2007 Late Quaternary vegetation fire and climate dynamics of Serra doAracatuba in the Atlantic coastal mountains of Paranaacute State southern BrazilVegetation History and Archaeobotany 1677ndash85

Behling H Arz HW Paumltzold J Wefer G 2002 Late Quaternary vegetational and climatedynamics in southeastern Brazil inferences from marine cores GeoB 3229-2 andGeoB 3202-1 Palaeogeography Palaeoclimatology Palaeoecology 179227ndash243DOI 101016S0031-0182(01)00435-7

Behling H Dupont L Safford HDWefer G 2007 Late Quaternary vegetation and cli-mate dynamics in the Serra da Bocaina southeastern Brazil Quaternary International16122ndash31 DOI 101016jquaint200610021

Behling H Lichte M 1997 Evidence of dry and cold climatic conditions at glacial timesin tropical southeastern Brazil Quaternary Research 48348ndash358DOI 101006qres19971932

Behling H Pillar V DePatta Bauermann SG 2005 Late Quaternary grassland (Cam-pos) gallery forest fire and climate dynamics studied by pollen charcoal andmultivariate analysis of the Satildeo Francisco de Assis core in western Rio Grande do Sul(southern Brazil) Review of Palaeobotany and Palynology 133235ndash248DOI 101016jrevpalbo200410004

Behling H Safford HD 2010 Late-glacial and Holocene vegetation climate and firedynamics in the Serra dos Oacutergatildeos Rio de Janeiro State southeastern Brazil GlobalChange Biology 161661ndash1671

BornscheinMR Belmonte-Lopes R Ribeiro LF Mauriacutecio GN Pie MR 2015 Rec-tification of the position of the type locality of Brachycephalus tridactylus (AnuraBrachycephalidae) a recently described species from southern Brazil Zootaxa4007149ndash150 DOI 1011646zootaxa4007114

BornscheinMR Correcirca L Belmonte-Lopes R Klemann Juacutenior L Caacuteceres NC Pie MR2012 The use of highlands by the Lowland Tapir (Tapirus terrestris) in the southernBrazilian Atlantic Forest Neotropical Biology and Conservation 7210ndash213


Brown JH Stevens GC Kaufman DM 1996 The geographic range size shape bound-aries and internal structure Annual Review of Ecology and Systematics 27597ndash623DOI 101146annurevecolsys271597

Brunes TO Sequeira F Haddad CFB Alexandrino J 2010 Gene and species trees ofa Neotropical group of treefrogs genetic diversification in the Brazilian AtlanticForest and the origin of a polyploid speciesMolecular Phylogenetics and Evolution571120ndash1133 DOI 101016jympev201008026

Campos LA 2011 Sistemaacutetica filogeneacutetica do gecircnero Brachycephalus Fitzinger 1826(Anura Brachycephalidae) com base em dados morfoloacutegicos Thesis BrasiacuteliaUniversidade de Brasiacutelia 67 p

Campos LA Silva HR da Sebben A 2010Morphology and development of additionalbony elements in the genus Brachycephalus (Anura Brachycephalidae) BiologicalJournal of the Linnean Society 99752ndash767 DOI 101111j1095-8312201001375x

Carnaval AC HickersonMJ Haddad CFB Rodrigues MT Moritz C 2009 Stability pre-dicts genetic diversity in the Brazilian Atlantic Forest hotspot Science 323785ndash789DOI 101126science1166955

Carvalho-e-Silva AMT de Silva GR da Carvalho-e-Silva SP de 2008 Anuros da ReservaRio das Pedras Mangaratiba RJ Brasil Biota Neotropica 8199ndash209DOI 101590S1676-06032008000100021

Clemente-Carvalho RBG Alves ACR Perez SI Haddad CFB Reis SF dos 2011aMorphological and molecular variation in the Pumpkin Toadlet Brachycephalusephippium (Anura Brachycephalidae) Journal of Herpetology 4594ndash99DOI 10167009-1641

Clemente-Carvalho RBG Antoniazzi MM Jared C Haddad CFB Alves ACR RochaHS Pereira GR Oliveira DF Lopes RT Reis SF dos 2009Hyperossification inminiaturized toadlets of the genus Brachycephalus (Amphibia Anura Brachy-cephalidae) microscopic structure and macroscopic patterns of variation Journalof Morphology 2701285ndash1295 DOI 101002jmor10755

Clemente-Carvalho RBG Giaretta AA Condez TH Haddad CFB Reis SF dos 2012 Anew species of miniaturized toadlet genus Brachycephalus (Anura Brachycephali-dae) from the Atlantic Forest of southeastern Brazil Herpetologica 68365ndash374DOI 101655HERPETOLOGICA-D-11-000851

Clemente-Carvalho RBG Klaczko J Perez SI Alves ACR Haddad CFB Reis SFdos 2011bMolecular phylogenetic relationships and phenotypic diversity inminiaturized toadlets genus Brachycephalus (Amphibia Anura Brachycephalidae)Molecular Phylogenetics and Evolution 6179ndash89 DOI 101016jympev201105017

Clemente-Carvalho RBG Monteiro LR Bonato V Rocha HS Pereira GR OliveiraDF Lopes RT Haddad CFB Martins EG Reis SF dos 2008 Geographic variationin cranial shape in the Pumpkin Toadlet (Brachycephalus ephippium) a geometricanalysis Journal of Herpetology 42176ndash185 DOI 10167007-141R11

Clemente-Carvalho RBG Perez SI Tonhatti CH Condez TH Sawaya RJ HaddadCFB Reis SF dos 2016 Boundaries of morphological and molecular variation and


the distribution range of a miniaturized froglet Brachycephalus nodoterga (AnuraBrachycephalidae) Journal of Herpetology 50169ndash178 DOI 10167014-119

Condez TH Clemente-Carvalho RBG Haddad CFB Reis SF dos 2014 A new species ofBrachycephalus (Anura Brachycephalidae) from the highlands of the Atlantic Forestsoutheastern Brazil Herpetologica 7089ndash99DOI 101655HERPETOLOGICA-D-13-00044

Condez TH Sawaya RJ DixoM 2009Herpetofauna dos remanescentes de MataAtlacircntica da regiatildeo de Tapiraiacute e Piedade SP sudeste do Brasil Biota Neotropica9157ndash185 DOI 101590S1676-06032009000300016

Corn PS 2005 Climate change and amphibians Animal Biodiversity and Conservation2859ndash67

Cruz CAG Feio RN 2007 Endemismos em anfiacutebios em aacutereas de altitudes na MataAtlacircntica no sudeste do Brasil In Nascimento LB Oliveira ME eds Herpetologiano Brasil II Belo Horizonte Sociedade Brasileira de Herpetologia 117ndash126

Cunha AK Oliveira IS de HartmannMT 2010 Anurofauna da Colocircnia Castelhanosna Aacuterea de Protecatildeo Ambiental de Guaratuba Serra do Mar paranaense BrasilBiotemas 23123ndash134

DixoM Verdade VK 2006Herpetofauna de serrapilheira da Reserva Florestal de MorroGrande Cotia (SP) Biota Neotropica 61ndash20

Dorigo TA Siqueira CC Vrcibradic D Maia-Carneiro T Almeida-Santos M RochaCFD 2012 Ecological aspects of the pumpkin toadlet Brachycephalus garbeanusMiranda-Ribeiro 1920 (Anura Neobatrachia Brachycephalidae) in a highlandforest of southeastern Brazil Journal of Natural History 462497ndash2507DOI 101080002229332012713525

Enters D Behling H Mayr C Dupont L Zolitschka B 2010Holocene environmentaldynamics of south-eastern Brazil recorded in laminated sediments of Lago AleixoJournal of Paleolimnology 44265ndash277 DOI 101007s10933-009-9402-z

Firkowski CR 2013 Diversification and microendemism in montane refugia from theBrazilian Atlantic Forest Dissertation Curitiba Universidade Federal do Paranaacute59 p

Fontoura PL Ribeiro LF Pie MR 2011 Diet of Brachycephalus brunneus (AnuraBrachycephalidae) in the Atlantic Rainforest of Paranaacute southern Brazil Zoologia28687ndash689 DOI 101590S1984-46702011000500019

Frost DR 2015 Amphibian species of the world 60 an ouline reference Availableat http researchamnhorgherpetologyamphibia indexhtml (accessed on 12September 2015)

GareyMV Lima AMX HartmannMT Haddad CFB 2012 A new species of miniatur-ized toadlet genus Brachycephalus (Anura Brachycephalidae) from southern BrazilHerpetologica 68266ndash271 DOI 101655HERPETOLOGICA-D-11-000741

Giaretta AA 1999 Diversidade e densidade de anuros de serapilheira num gradientealtitudinal na mata atlacircntica costeira Thesis Campinas Universidade Estadual deCampinas 140 p


Giaretta AA Facure KG Sawaya RJ Meyer JH deM Chemin N 1999 Diversity andabundance of litter frogs in a montane forest of Southeastern Brazil seasonal andaltitudinal changes Biotropica 31669ndash674 DOI 101111j1744-74291999tb00416x

Giaretta AA Sawaya RJ 1998 Second species of Psyllophryne (Anura Brachycephali-dae) Copeia 1998985ndash987 DOI 1023071447345

Giaretta AA Sawaya RJ Machado G ArauacutejoMS Facure KG Medeiros HF de NunesR 1997 Diversity and abundance of litter frogs at altitudinal sites at Serra do JapiSoutheastern Brazil Revista Brasileira de Zoologia 14341ndash346DOI 101590S0101-81751997000200008

Giarla TC Voss RS Jansa SA 2014Hidden diversity in the Andes comparison ofspecies delimitation methods in montane marsupialsMolecular Phylogenetics andEvolution 70137ndash151 DOI 101016jympev201309019

Haddad CFB Alves ACR Clemente-Carvalho RBG Reis SF dos 2010 A new species ofBrachycephalus from the Atlantic Rain Forest in Satildeo Paulo state southeastern Brazil(Amphibia Anura Brachycephalidae) Copeia 2010410ndash420DOI 101643CH-09-102

Hanken J Wake DB 1993Miniaturization of body size organismal consequences andevolutionary significance Annual Review of Ecology and Systematics 24501ndash519DOI 101146annureves24110193002441

Hessler I Dupont L Bonnefille R Behling H Gonzaacutelez C Helmens KF HooghiemstraH Lebamba J LedruM-P Leacutezine A-M Maley J Marret F Vincens A 2010Millennial-scale changes in vegetation records from tropical Africa and SouthAmerica during the last glacial Quaternary Science Reviews 292882ndash2899DOI 101016jquascirev200911029

IBGE 1993Mapa de unidades de relevo do Brasil Rio de Janeiro Instituto Brasileiro deGeografia e EstatiacutesticamdashIBGE


IUCN 2012 IUCN Red List categories and criteria Second edition Version 31 GlandInternational Union for Conservation of NaturemdashIUCN

Izecksohn E 1971 Novo gecircnero e nova espeacutecie de Brachycephalidae do Estado do Rio deJaneiro Brasil Boletim do Museu Nacional Zoologia 2801ndash12

Jump AS Huang TJ Chou CH 2012 Rapid altitudinal migration of mountain plants inTaiwan and its implications for high altitude biodiversity Ecography 35204ndash210DOI 101111j1600-0587201106984x

Kaplan K 2002Histology of the anteroventral part of the breast-shoulder apparatus ofBrachycephalus ephippium (Brachycephalidae) with comments on the validity of thegenus Psyllophryne (Brachycephalidae) Amphibia-Reptilia 23225ndash227

Knyazhnitskiy OV Monk RR Parker NC Baker RJ 2000 Assignment of GlobalInformation System coordinates to classical museum localities for relational databaseanalyses Occasional Papers 1991ndash15

Langone JA Segalla MV BornscheinM Saacute RO de 2008 A new reproductive mode inthe genusMelanophryniscus Gallardo 1961 (Anura Bufonidae) with description of


a new species from the state of Paranaacute Brazil South American Journal of Herpetology31ndash9 DOI 1029941808-9798(2008)3[1ANRMIT]20CO2

Maack R 1981 Geografia fiacutesica do estado do Paranaacute In Rio de Janeiro Livraria JoseacuteOlympio Editora 450 p

Mariotto LR 2014 Anfiacutebios de um gradiente altitudinal em mata atlacircntica DissertationCuritiba Universidade Federal do Paranaacute 174 p

Mata H Fontana CS Mauriacutecio GN BornscheinMR Vasconcelos MF de BonattoSL 2009Molecular phylogeny and biogeography of the eastern Tapaculos (AvesRhinocryptidae Scytalopus Eleoscytalopus) Cryptic diversification in BrazilianAtlantic ForestMolecular Phylogenetics and Evolution 53450ndash462DOI 101016jympev200907017

Mauriacutecio GN Belmonte-Lopes R Pacheco JF Silveira LFWhitney BM BornscheinMR 2014 Taxonomy of lsquolsquoMouse-colored Tapaculosrsquorsquo (II) an endangered newspecies from the montane Atlantic Forest of southern Bahia Brazil (PasseriformesRhinocryptidae Scytalopus) The Auk 131643ndash659 DOI 101642AUK-14-161

Mauriacutecio GN BornscheinMR Vasconcelos MF de Whitney BM Pacheco JF SilveiraLF 2010 Taxonomy of lsquolsquoMouse-colored Tapaculosrsquorsquo I On the application of thenameMalacorhynchus speluncae Meacuteneacutetrieacutes 1835 (Aves Passeriformes Rhinocrypti-dae) Zootaxa 251832ndash48

Miranda-Ribeiro A de 1920 Os brachycephalideos do Museu Paulista (com tres especiesnovas) Revista do Museu Paulista 12306ndash318

MMA 2016 Brazilian Ministry of environment spatial data Available at httpmapasmmagovbr i3geodatadownloadhtm

Mohr C 1947 Table of equivalent populations of North American small mammalsAmerican Midland Naturalist 37223ndash249 DOI 1023072421652

Napoli MF Caramaschi U Cruz CAG Dias IR 2011 A new species of flea-toad genusBrachycephalus Fitzinger (Amphibia Anura Brachycephalidae) from the Atlanticrainforest of southern Bahia Brazil Zootaxa 273933ndash40DOI 1011646zootaxa273913

Oliveira EG de 2013Histoacuteria natural de Brachycephalus pitanga no Nuacutecleo SantaVirgiacutenia Parque Estadual da Serra do Mar Estado de Satildeo Paulo Dissertation RioClaro Universidade Estadual Paulista lsquolsquoJuacutelio de Mesquita Filhorsquorsquo 78 p

Oliveira JCF de Coco L Pagotto RV Pralon E Vrcibradic D Pombal Jr JP Rocha CFD2012 Amphibia Anura Brachycephalus didactylus (Izecksohn 1971) and Zachaenusparvulus (Girard 1853) distribution extension Check List 8242ndash244DOI 101556082242

Oliveira EG de Haddad CFB 2015 Diet seasonality and feeding preferences of Brachy-cephalus pitanga (Anura Brachycephalidae) Journal of Herpetology 49252ndash256DOI 10167013-211

Oliveira AKC de Oliveira IS de HartmannMT Silva NR da Toledo LF 2011 Am-phibia Anura Brachycephalidae Brachycephalus hermogenesi (Giaretta amp Sawaya1998) new species record in the state of Paranaacute southern Brazil and geographicdistribution map Check List 717ndash18


Oliveira JCF Pralon E Coco L Pagotto RV Rocha CFD 2013 Environmental humidityand leaf-litter depth affecting ecological parameters of a leaf-litter frog community inan Atlantic Rainforest area Journal of Natural History 472115ndash2124DOI 101080002229332013769641

Padial JM Grant T Frost DR 2014Molecular systematics of terraranas (AnuraBrachycephaloidea) with an assessment of the effects of alignment and optimalitycriteria Zootaxa 38251ndash132 DOI 1011646zootaxa382511

Paacuteez-Moscoso DJ Guayasamin JM 2012 Species limits in the Andean toad genusOsornophryne (Bufonidae)Molecular Phylogenetics and Evolution 65805ndash822DOI 101016jympev201208001

Pereira M dos S Candaten A Milani D Oliveira FB de Gardelin J Rocha CFDVrcibradic D 2010 Brachycephalus hermogenesi Herpetological Review 41506

Pie MR Meyer ALS Firkowski CR Ribeiro LF BornscheinMR 2013 Understandingthe mechanisms underlying the distribution of microendemic montane frogs(Brachycephalus spp Terrarana Brachycephalidae) in the Brazilian AtlanticRainforest Ecological Modelling 250165ndash176 DOI 101016jecolmodel201210019

Pie MR Ribeiro LF 2015 A new species of Brachycephalus (Anura Brachycephalidae)from the Quiriri mountain range of southern Brazil PeerJ 3e1179DOI 107717peerj1179

Pimenta BVS Beacuternils RS Pombal Jr JP 2007 Amphibia Anura BrachycephalidaeBrachycephalus hermogenesi filling gap and geographic distribution map Check List3277ndash279 DOI 101556033277

Pires Jr OR Sebben A Schwartz EF Bloch Jr C Morales RAV Schwartz CA 2003The occurrence of 11-oxotetrodotoxin a rare tetrodotoxin analogue in the brachy-cephalidae (sic) frog Brachycephalus ephippium Toxicon 42563ndash566DOI 101016S0041-0101(03)00235-6

Pires Jr OR Sebben A Schwartz EF Largura SWR Bloch Jr C Morales RAV SchwartzCA 2002 Occurrence of tetrodotoxin and its analogues in the Brazilian frogBrachycephalus ephippium (Anura Brachycephalidae) Toxicon 40761ndash766DOI 101016S0041-0101(01)00279-3

Pires Jr OR Sebben A Schwartz EF Morales RAV Bloch Jr C Schwartz CA 2005Further report of the occurrence of tetrodotoxin and new analogues in the Anuranfamily Brachycephalidae Toxicon 4573ndash79 DOI 101016jtoxicon200409016

Pombal Jr JP 1999 Oviposicatildeo e desenvolvimento de Brachycephalus ephippium (Spix)(Anura Brachycephalidae) Revista Brasileira de Zoologia 16967ndash976DOI 101590S0101-81751999000400004

Pombal Jr JP 2001 A new species of Brachycephalus (Anura Brachycephalidae) fromAtlantic Forest of southeastern Brazil Amphibia-Reptilia 22179ndash185DOI 10116315685380152030409

Pombal Jr JP 2010 A posicatildeo taxonocircmica das variedades de Brachycephalus ephippium(Spix 1824) descritas por (Miranda-Ribeiro 1920) (Amphibia Anura Brachy-cephalidae) Boletim do Museu Nacional Zoologia 5261ndash12


Pombal Jr JP Gasparini JL 2006 A new Brachycephalus (Anura Brachycephalidae) fromthe Atlantic Rainforest of Espiacuterito Santo southeastern Brazil South American Journalof Herpetology 187ndash93 DOI 1029941808-9798(2006)1[87ANBABF]20CO2

Pombal Jr JP Izecksohn E 2011 Uma nova espeacutecie de Brachycephalus (Anura Brachy-cephalidae) do Estado do Rio de Janeiro Papeacuteis Avulsos de Zoologia 51443ndash451

Pombal Jr JP Sazima I Haddad CFB 1994 Breeding behavior of the pumpkin toadletBrachycephalus ephippium (Brachycephalidae) Journal of Herpetology 28516ndash519DOI 1023071564972

Pombal Jr JP Wistuba EM BornscheinMR 1998 A new species of brachycephalid(Anura) from the Atlantic Rain Forest of Brazil Journal of Herpetology 3270ndash74DOI 1023071565481

Reinert BL BornscheinMR Firkowski C 2007 Distribuicatildeo tamanho populacionalhaacutebitat e conservacatildeo do bicudinho-do-brejo Stymphalornis acutirostris BornscheinReinert e Teixeira 1995 (Thamnophilidae) Revista Brasileira de Ornitologia15493ndash519

Ribeiro R da S 2006 Ecologia alimentar das quatro espeacutecies dominantes da anurofaunade serapilheira em um gradiente altitudinal na ilha de Satildeo Sebastiatildeo SP DissertationRio Claro Universidade Estadual Paulista Juacutelio de Mesquita Filho 124 p

Ribeiro LF Alves ACR Haddad CFB Reis SF dos 2005 Two new species of Brachy-cephalus Guumlnther 1858 from the state of Paranaacute southern Brazil (Amphibia AnuraBrachycephalidae) Boletim do Museu Nacional Zoologia 5191ndash18

Ribeiro LF BornscheinMR Belmonte-Lopes R Firkowski CR Morato SAA Pie MR2015 Seven new microendemic species of Brachycephalus (Anura Brachycephalidae)from southern Brazil PeerJ 3e1011 DOI 107717peerj1011

Ribeiro LF Stroumlher PR Firkowski CR Cini FA BornscheinMR Pie MR 2014 Brachy-cephalus pernix (Anura Brachycephalidae) a new host of Ophiotaenia (EucestodaProteocephalidea) Herpetology Notes 7291ndash294

Rocha CFD Van Sluys M Alves MAS Bergallo HG Vrcibradic D 2000 Activity ofleaf-litter frogs When should frogs be sampled Journal of Herpetology 34285ndash287DOI 1023071565426

Rocha CFD Van Sluys M Alves MAS Bergallo HG Vrcibradic D 2001 Estimates offorest floor litter frog communities a comparison of two methods Austral Ecology2614ndash21

Rocha CFD Vrcibradic D Kiefer MC Almeida-GomesM Borges-Junior VNTMenezes VA Ariani CV Pontes JAL Goyannes-Arauacutejo P Marra RV Guedes DMSiqueira C da C Van Sluys M 2013 The leaf-litter frog community from ReservaRio das Pedras Mangaratiba Rio de Janeiro State Southeastern Brazil speciesrichness composition and densities North-Western Journal of Zoology 9151ndash156

Santos-Pereira M Candaten A Milani D Oliveira FB Gardelin J Rocha CFD da 2011Seasonal variation in the leaf-litter frog community (Amphibia Anura) from anAtlantic Forest area in the Salto Morato Natural Reserve southern Brazil Zoologia28755ndash761 DOI 101590S1984-46702011000600008


Schwartz CA CastroM de S Pires Juacutenior OR Maciel NM Schwartz ENF SebbenA 2007 Princiacutepios bioativos da pele de anfiacutebios panorama atual e perspectivasIn Nascimento LB Oliveira ME eds Herpetologia no Brasil II Belo HorizonteSociedade Brasileira de Herpetologia 146ndash168

Sebben A Schwartz CA Valente D Mendes EG 1986 A tetrodotoxin-like substancefound in the Brazilian frog Brachycephalus ephippium Toxicon 24799ndash806DOI 1010160041-0101(86)90105-4

Silva HR da Campos LA Sebben A 2007 The auditory region of Brachycephalus andits bearing on the monophyly of the genus (Anura Brachycephalidae) Zootaxa142259ndash68

Siqueira CC Vrcibradic D Almeida-GomesM Borges Jr VNT Almeida-Santos PAlmeida-Santos M Ariani CV Guedes DM Goyannes-Arauacutejo P Dorigo TA VanSluys M Rocha CFD 2009 Density and richness of the leaf litter frogs of an AtlanticRainforest area in Serra dos Oacutergatildeos Rio de Janeiro State Brazil Zoologia 2697ndash102DOI 102108zsj2697

Siqueira CC Vrcibradic D Dorigo TA Rocha CFD 2011 Anurans from two high-elevation areas of Atlantic Forest in the state of Rio de Janeiro Brazil Zoologia28457ndash464 DOI 101590S1984-46702011000400007

Siqueira CC Vrcibradic D Nogueira-Costa P Martins AR Dantas L Gomes VLRBergallo HG Rocha CFD 2014 Environmental parameters affecting the structureof leaf-litter frog (Amphibia Anura) communities in tropical forests a case studyfrom an Atlantic Rainforest area in southeastern Brazil Zoologia 31147ndash152DOI 101590S1984-46702014000200005

Siqueira CC Vrcibradic D Rocha CFD 2013 Altitudinal records of data-deficientand threatened frog species from the Atlantic Rainforest of the Serra dos Oacutergatildeosmountains in southeastern Brazil Brazilian Journal of Biology 73229ndash230DOI 101590S1519-69842013000100027

Struminski E 1997 Parque Estadual Pico do Marumbi estudo de vegetacatildeo e anaacutelise deaacutereas de instabilidade ambiental Agraacuterias 16107ndash119

Tandel M da CFF Loibel S Oliveira EG de Haddad CFB 2014 Diferenciacatildeo de 3 tiposde vocalizacotildees (cantos) na espeacutecie Brachycephalus pitanga Revista da Estatiacutestica daUniversidade Federal de Ouro Preto 3374ndash386

ThomeacuteMTC Zamudio KR Giovanelli JGR Haddad CFB Baldissera Jr FA Alexan-drino J 2010 Phylogeography of endemic toads and post-Pliocene persistence of theBrazilian Atlantic ForestMolecular Phylogenetics and Evolution 551018ndash1031DOI 101016jympev201002003

Trevine V Forlani MC Haddad CFB Zaher H 2014Herpetofauna of Paranapiacabaexpanding our knowledge on a historical region in the Atlantic forest of southeasternBrazil Zoologia 31126ndash146 DOI 101590S1984-46702014000200004

Van Sluys M Vrcibradic D Alves MAS Bergallo HG Rocha CFD 2007 Ecologicalparameters of the leaf-litter frog community of an Atlantic Rainforest area at IlhaGrande Rio de Janeiro state Brazil Austral Ecology 32254ndash260DOI 101111j1442-9993200701682x


Veloso HP Rangel-Filho ALR Lima JCA 1991 Classificacatildeo da vegetacatildeo brasileiraadaptada a um sistema universal Rio de Janeiro Instituto Brasileiro de Geografia eEstatiacutestica ndashIBGE 123 p

Verdade VK Rodrigues MT Cassimiro J Pavan D Liou N LangeM 2008 Advertise-ment call vocal activity and geographic distribution of Brachycephalus hermogenesi(Giaretta amp Sawaya 1998) (Anura Brachycephalidae) Journal of Herpetology42542ndash549 DOI 10167007-2871

Walter H 1977 Zonas de vegetacioacuten y clima Barcelona Ediciones Omega 245 pWieczorek J Guo Q Hijmans RJ 2004 The point-radius method for georeferencing

locality descriptions and calculating associated uncertainty International Journal ofGeographical Information Science 18745ndash767 DOI 10108013658810412331280211

Wistuba EM 1998Histoacuteria natural de Brachycephalus pernix Pombal Wistuba andBornschein 1998 (Anura) no Morro Anhangava Municiacutepio de Quatro BarrasEstado do Paranaacute Dissertation Curitiba Universidade Federal do Paranaacute 89 p

Wollenberg KC Vieites DR Glaw F Vences M 2011 Speciation in little the roleof range and body size in the diversification of Malagasy mantellid frogs BMCEvolutionary Biology 11217 DOI 1011861471-2148-11-217

Yeh J 2002 The effect of miniaturized body size on skeletal morphology in frogsEvolution 56628ndash641 DOI 101111j0014-38202002tb01372x

Zaher H Aguiar E Pombal JP 2005 Paratelmatobius gaigeae (Cochran 1938) rediscov-ered (Amphibia Anura Leptodactylidae) Arquivos do Museu Nacional 63321ndash328


845 m asl in the state of Paranaacute and at 455 m asl in the state of Santa CatarinaThe altitudinal occurrence in the pernix species group seems to decrease southwardSyntopy between species is also reviewed

Subjects Biodiversity Biogeography ZoologyKeywords Cloud forest Highlands Relief units Syntopy Species group Extent of occurrence

INTRODUCTIONBrachycephalus Fitzinger is a genus of miniaturized diurnal toadlets (usually lt25 cm insnout-vent length) that inhabit the forest floor of montane regions along the AtlanticRainforest of southeastern and southern Brazil (Izecksohn 1971 Giaretta amp Sawaya 1998Pombal Jr Wistuba amp Bornschein 1998 Napoli et al 2011 Pie et al 2013 see Rocha et al(2000) and Pombal Jr amp Izecksohn (2011) for reports of nocturnal activity) Brachycephaluspresents direct development and a reduction in the number and size of digits (Hanken ampWake 1993 Pombal Jr 1999 Yeh 2002) Some species are aposematic (yellow orangeor yellow with light red) of which some were confirmed as harboring neurotoxins(tetrodotoxin and analogues Sebben et al 1986 Pires Jr et al 2002 Pires Jr et al 2003Schwartz et al 2007)

Recently Kaplan (2002) proposed that the genus Psyllophryne Izecksohn should beconsidered as a junior synonym of Brachycephalus Psyllophryne included two speciesP didactyla and P hermogenesi lsquolsquowith dorsal surfaces brown tiny body sizes (snout-ventlength 86ndash102 mm) body leptodactyliform and long-distance jumpersrsquorsquo (Napoli et al2011) There are currently 29 described species of Brachycephalus (Frost 2015 see Pie ampRibeiro 2015 Ribeiro et al 2015) and although 20 of them were described within the last10 years it is likely that many more species are still waiting to be described Moreoverecological data on species of the genusBrachycephalus is still limited To date it only includesdata on the breeding behavior of B ephippium (Pombal Jr Sazima amp Haddad 1994 PombalJr 1999) vocal activity of B hermogenesi (Verdade et al 2008) advertisement calls of Bephippium (Pombal Jr Sazima amp Haddad 1994) B hermogenesi (Verdade et al 2008) Bpitanga (Arauacutejo et al 2012) B tridactylus (Garey et al 2012) and B crispus (Condez et al2014) abundance estimates of B didactylus (Van Sluys et al 2007 Almeida-Santos et al2011 Rocha et al 2013 Siqueira et al 2014) and its diet (Almeida-Santos et al 2011) thediet of B brunneus (Fontoura Ribeiro amp Pie 2011) B garbeanus (Dorigo et al 2012) andB pitanga (Oliveira amp Haddad 2015) and microhabitat preference of B garbeanus (Dorigoet al 2012)

A recently-proposed phylogenetic hypothesis for the genus indicated their separationinto three main clades with still some uncertainty regarding relationships within eachclade (Clemente-Carvalho et al 2011b) Based on the species studied by Clemente-Carvalho et al (2011b) one clade included B didactylus and B hermogenesi a secondclade included B brunneus B ferruginus B izecksohni B pernix and B pombali anda third clade included B alipioi B ephippium B garbeanus B nodoterga B pitangaB toby and B vertebralis Two morphological traitsmdashthe presenceabsence of dermal


























































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Table 1 (continued)










Brachycephalussp 1



Brachycephalussp 1



Brachycephalussp 1



Brachycephalussp 1



Brachycephalussp 1



Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1





Bornschein

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Table 1 (continued)


Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1









ES (1430) Pie et al (2013)






SP 800-1100 Condez et al (2014)






SP 1225 Pie et al (2013)



SP 700 Pie et al (2013)



RJ 750 Pie et al (2013)


Bornschein

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Table 1 (continued)




RJ 1125 Pie et al (2013)


































Bornschein

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Table 1 (continued)






















RJ 1195 Pie et al (2013)



RJ 950 Pie et al (2013)


























Bornschein

etal(2016)PeerJDO

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Table 1 (continued)





























B margarita-tus




B margarita-tus




B margarita-tus




B margarita-tus





Bornschein

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Table 1 (continued)


B margarita-tus




B margarita-tus


























Bornschein

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Table 1 (continued)














Brachycephalussp 2




Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



B aurogutta-tus











Bornschein

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Table 1 (continued)




















B fuscolinea-tus

Leste Catari-nense












B





Bornschein

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Table 1 (continued)
































Brachycephalussp 4




Brachycephalussp 4




Brachycephalussp 5





Bornschein

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Table 1 (continued)


Brachycephalussp 5




Brachycephalussp 6




Excluded recordsf





















Bornschein

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Table 1 (continued)






























B margarita-tus




B cfmargari-tatus








Bornschein

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Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




Bornschein

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Table 1 (continued)








Bornschein

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Bornschein

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Table 1 (continued)










Brachycephalussp 1



Brachycephalussp 1



Brachycephalussp 1



Brachycephalussp 1



Brachycephalussp 1



Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1





Bornschein

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Table 1 (continued)


Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1









ES (1430) Pie et al (2013)






SP 800-1100 Condez et al (2014)






SP 1225 Pie et al (2013)



SP 700 Pie et al (2013)



RJ 750 Pie et al (2013)


Bornschein

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Table 1 (continued)




RJ 1125 Pie et al (2013)


































Bornschein

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Table 1 (continued)






















RJ 1195 Pie et al (2013)



RJ 950 Pie et al (2013)


























Bornschein

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Table 1 (continued)





























B margarita-tus




B margarita-tus




B margarita-tus




B margarita-tus





Bornschein

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Table 1 (continued)


B margarita-tus




B margarita-tus


























Bornschein

etal(2016)PeerJDO

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Table 1 (continued)














Brachycephalussp 2




Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



B aurogutta-tus











Bornschein

etal(2016)PeerJDO

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Table 1 (continued)




















B fuscolinea-tus

Leste Catari-nense












B





Bornschein

etal(2016)PeerJDO

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Table 1 (continued)
































Brachycephalussp 4




Brachycephalussp 4




Brachycephalussp 5





Bornschein

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Table 1 (continued)


Brachycephalussp 5




Brachycephalussp 6




Excluded recordsf





















Bornschein

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Table 1 (continued)






























B margarita-tus




B cfmargari-tatus








Bornschein

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Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




Bornschein

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Table 1 (continued)








Bornschein

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Table 1 (continued)










Brachycephalussp 1



Brachycephalussp 1



Brachycephalussp 1



Brachycephalussp 1



Brachycephalussp 1



Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1





Bornschein

etal(2016)PeerJDO

I107717peerj2490841

Table 1 (continued)


Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1









ES (1430) Pie et al (2013)






SP 800-1100 Condez et al (2014)






SP 1225 Pie et al (2013)



SP 700 Pie et al (2013)



RJ 750 Pie et al (2013)


Bornschein

etal(2016)PeerJDO

I107717peerj2490941

Table 1 (continued)




RJ 1125 Pie et al (2013)


































Bornschein

etal(2016)PeerJDO

I107717peerj24901041

Table 1 (continued)






















RJ 1195 Pie et al (2013)



RJ 950 Pie et al (2013)


























Bornschein

etal(2016)PeerJDO

I107717peerj24901141

Table 1 (continued)





























B margarita-tus




B margarita-tus




B margarita-tus




B margarita-tus





Bornschein

etal(2016)PeerJDO

I107717peerj24901241

Table 1 (continued)


B margarita-tus




B margarita-tus


























Bornschein

etal(2016)PeerJDO

I107717peerj24901341

Table 1 (continued)














Brachycephalussp 2




Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



B aurogutta-tus











Bornschein

etal(2016)PeerJDO

I107717peerj24901441

Table 1 (continued)




















B fuscolinea-tus

Leste Catari-nense












B





Bornschein

etal(2016)PeerJDO

I107717peerj24901541

Table 1 (continued)
































Brachycephalussp 4




Brachycephalussp 4




Brachycephalussp 5





Bornschein

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I107717peerj24901641

Table 1 (continued)


Brachycephalussp 5




Brachycephalussp 6




Excluded recordsf





















Bornschein

etal(2016)PeerJDO

I107717peerj24901741

Table 1 (continued)






























B margarita-tus




B cfmargari-tatus








Bornschein

etal(2016)PeerJDO

I107717peerj24901841

Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




Bornschein

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Table 1 (continued)








Bornschein

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Table 1 (continued)


Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1




Brachycephalussp 1









ES (1430) Pie et al (2013)






SP 800-1100 Condez et al (2014)






SP 1225 Pie et al (2013)



SP 700 Pie et al (2013)



RJ 750 Pie et al (2013)


Bornschein

etal(2016)PeerJDO

I107717peerj2490941

Table 1 (continued)




RJ 1125 Pie et al (2013)


































Bornschein

etal(2016)PeerJDO

I107717peerj24901041

Table 1 (continued)






















RJ 1195 Pie et al (2013)



RJ 950 Pie et al (2013)


























Bornschein

etal(2016)PeerJDO

I107717peerj24901141

Table 1 (continued)





























B margarita-tus




B margarita-tus




B margarita-tus




B margarita-tus





Bornschein

etal(2016)PeerJDO

I107717peerj24901241

Table 1 (continued)


B margarita-tus




B margarita-tus


























Bornschein

etal(2016)PeerJDO

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Table 1 (continued)














Brachycephalussp 2




Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



B aurogutta-tus











Bornschein

etal(2016)PeerJDO

I107717peerj24901441

Table 1 (continued)




















B fuscolinea-tus

Leste Catari-nense












B





Bornschein

etal(2016)PeerJDO

I107717peerj24901541

Table 1 (continued)
































Brachycephalussp 4




Brachycephalussp 4




Brachycephalussp 5





Bornschein

etal(2016)PeerJDO

I107717peerj24901641

Table 1 (continued)


Brachycephalussp 5




Brachycephalussp 6




Excluded recordsf





















Bornschein

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Table 1 (continued)






























B margarita-tus




B cfmargari-tatus








Bornschein

etal(2016)PeerJDO

I107717peerj24901841

Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




Bornschein

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Table 1 (continued)








Bornschein

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Table 1 (continued)




RJ 1125 Pie et al (2013)


































Bornschein

etal(2016)PeerJDO

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Table 1 (continued)






















RJ 1195 Pie et al (2013)



RJ 950 Pie et al (2013)


























Bornschein

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I107717peerj24901141

Table 1 (continued)





























B margarita-tus




B margarita-tus




B margarita-tus




B margarita-tus





Bornschein

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I107717peerj24901241

Table 1 (continued)


B margarita-tus




B margarita-tus


























Bornschein

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Table 1 (continued)














Brachycephalussp 2




Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



B aurogutta-tus











Bornschein

etal(2016)PeerJDO

I107717peerj24901441

Table 1 (continued)




















B fuscolinea-tus

Leste Catari-nense












B





Bornschein

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Table 1 (continued)
































Brachycephalussp 4




Brachycephalussp 4




Brachycephalussp 5





Bornschein

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Table 1 (continued)


Brachycephalussp 5




Brachycephalussp 6




Excluded recordsf





















Bornschein

etal(2016)PeerJDO

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Table 1 (continued)






























B margarita-tus




B cfmargari-tatus








Bornschein

etal(2016)PeerJDO

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Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




Bornschein

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Table 1 (continued)








Bornschein

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Table 1 (continued)






















RJ 1195 Pie et al (2013)



RJ 950 Pie et al (2013)


























Bornschein

etal(2016)PeerJDO

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Table 1 (continued)





























B margarita-tus




B margarita-tus




B margarita-tus




B margarita-tus





Bornschein

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Table 1 (continued)


B margarita-tus




B margarita-tus


























Bornschein

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Table 1 (continued)














Brachycephalussp 2




Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



B aurogutta-tus











Bornschein

etal(2016)PeerJDO

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Table 1 (continued)




















B fuscolinea-tus

Leste Catari-nense












B





Bornschein

etal(2016)PeerJDO

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Table 1 (continued)
































Brachycephalussp 4




Brachycephalussp 4




Brachycephalussp 5





Bornschein

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Table 1 (continued)


Brachycephalussp 5




Brachycephalussp 6




Excluded recordsf





















Bornschein

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Table 1 (continued)






























B margarita-tus




B cfmargari-tatus








Bornschein

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Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




Bornschein

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Table 1 (continued)








Bornschein

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Table 1 (continued)





























B margarita-tus




B margarita-tus




B margarita-tus




B margarita-tus





Bornschein

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Table 1 (continued)


B margarita-tus




B margarita-tus


























Bornschein

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Table 1 (continued)














Brachycephalussp 2




Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



B aurogutta-tus











Bornschein

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Table 1 (continued)




















B fuscolinea-tus

Leste Catari-nense












B





Bornschein

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Table 1 (continued)
































Brachycephalussp 4




Brachycephalussp 4




Brachycephalussp 5





Bornschein

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Table 1 (continued)


Brachycephalussp 5




Brachycephalussp 6




Excluded recordsf





















Bornschein

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Table 1 (continued)






























B margarita-tus




B cfmargari-tatus








Bornschein

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Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




Bornschein

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Table 1 (continued)








Bornschein

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Table 1 (continued)


B margarita-tus




B margarita-tus


























Bornschein

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Table 1 (continued)














Brachycephalussp 2




Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



B aurogutta-tus











Bornschein

etal(2016)PeerJDO

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Table 1 (continued)




















B fuscolinea-tus

Leste Catari-nense












B





Bornschein

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Table 1 (continued)
































Brachycephalussp 4




Brachycephalussp 4




Brachycephalussp 5





Bornschein

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Table 1 (continued)


Brachycephalussp 5




Brachycephalussp 6




Excluded recordsf





















Bornschein

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Table 1 (continued)






























B margarita-tus




B cfmargari-tatus








Bornschein

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Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




Bornschein

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Table 1 (continued)








Bornschein

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Table 1 (continued)














Brachycephalussp 2




Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



Brachycephalussp 3

Central Serrado Mar



B aurogutta-tus











Bornschein

etal(2016)PeerJDO

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Table 1 (continued)




















B fuscolinea-tus

Leste Catari-nense












B





Bornschein

etal(2016)PeerJDO

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Table 1 (continued)
































Brachycephalussp 4




Brachycephalussp 4




Brachycephalussp 5





Bornschein

etal(2016)PeerJDO

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Table 1 (continued)


Brachycephalussp 5




Brachycephalussp 6




Excluded recordsf





















Bornschein

etal(2016)PeerJDO

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Table 1 (continued)






























B margarita-tus




B cfmargari-tatus








Bornschein

etal(2016)PeerJDO

I107717peerj24901841

Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




Bornschein

etal(2016)PeerJDO

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Table 1 (continued)








Bornschein

etal(2016)PeerJDO

I107717peerj24902041












































































































































































































Table 1 (continued)




















B fuscolinea-tus

Leste Catari-nense












B





Bornschein

etal(2016)PeerJDO

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Table 1 (continued)
































Brachycephalussp 4




Brachycephalussp 4




Brachycephalussp 5





Bornschein

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Table 1 (continued)


Brachycephalussp 5




Brachycephalussp 6




Excluded recordsf





















Bornschein

etal(2016)PeerJDO

I107717peerj24901741

Table 1 (continued)






























B margarita-tus




B cfmargari-tatus








Bornschein

etal(2016)PeerJDO

I107717peerj24901841

Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




Bornschein

etal(2016)PeerJDO

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Table 1 (continued)








Bornschein

etal(2016)PeerJDO

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Table 1 (continued)
































Brachycephalussp 4




Brachycephalussp 4




Brachycephalussp 5





Bornschein

etal(2016)PeerJDO

I107717peerj24901641

Table 1 (continued)


Brachycephalussp 5




Brachycephalussp 6




Excluded recordsf





















Bornschein

etal(2016)PeerJDO

I107717peerj24901741

Table 1 (continued)






























B margarita-tus




B cfmargari-tatus








Bornschein

etal(2016)PeerJDO

I107717peerj24901841

Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




Bornschein

etal(2016)PeerJDO

I107717peerj24901941

Table 1 (continued)








Bornschein

etal(2016)PeerJDO

I107717peerj24902041












































































































































































































Table 1 (continued)


Brachycephalussp 5




Brachycephalussp 6




Excluded recordsf





















Bornschein

etal(2016)PeerJDO

I107717peerj24901741

Table 1 (continued)






























B margarita-tus




B cfmargari-tatus








Bornschein

etal(2016)PeerJDO

I107717peerj24901841

Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




Bornschein

etal(2016)PeerJDO

I107717peerj24901941

Table 1 (continued)








Bornschein

etal(2016)PeerJDO

I107717peerj24902041












































































































































































































Table 1 (continued)






























B margarita-tus




B cfmargari-tatus








Bornschein

etal(2016)PeerJDO

I107717peerj24901841

Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




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etal(2016)PeerJDO

I107717peerj24901941

Table 1 (continued)








Bornschein

etal(2016)PeerJDO

I107717peerj24902041












































































































































































































Table 1 (continued)








Brachycephalussp 7

Central Serrado Mar
















Central Serrado Mar




Bornschein

etal(2016)PeerJDO

I107717peerj24901941

Table 1 (continued)








Bornschein

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Table 1 (continued)








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geographical and altitudinal distribution of ... · 6 stcp engenharia de projetos ltda., curitiba,...

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