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<mods:title id="F089CE7CE02541B4D5B698E5E29B6D3C">Larval chondrocranium morphology of five species of Proceratophrys Miranda-Ribeiro (Amphibia; Anura; Odontophrynidae)</mods:title>
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<mods:namePart id="A3E471E289CB3EDB3004361EBD2568C8">Dias, Pedro Henrique Dos Santos</mods:namePart>
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<mods:namePart id="A8999ABCFE1595F155A566CF15334580">Carvalho-E-Silva, Ana Maria Paulino Telles De</mods:namePart>
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<mods:namePart id="9EBB02E52F3D579CB82630D704BE1D1D">Carvalho-E-Silva, Sergio Potsch De</mods:namePart>
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<paragraph id="531536A7FFC98F4BFF01FB08FDD5FB58" blockId="7.[151,590,1195,1222]" box="[151,590,1195,1222]" pageId="7" pageNumber="434">
<heading id="085D81CBFFC98F4BFF01FB08FDD5FB58" bold="true" box="[151,590,1195,1222]" fontSize="11" level="1" pageId="7" pageNumber="434" reason="1">
<emphasis id="61DEEAB5FFC98F4BFF01FB08FDD5FB58" bold="true" box="[151,590,1195,1222]" pageId="7" pageNumber="434">
The 
<taxonomicName id="94AA4D24FFC98F4BFF59FB0FFE50FB5B" box="[207,459,1196,1222]" class="Amphibia" family="Cycloramphidae" genus="Proceratophrys" kingdom="Animalia" order="Anura" pageId="7" pageNumber="434" phylum="Chordata" rank="species" species="boiei">
<emphasis id="61DEEAB5FFC98F4BFF59FB0FFE50FB5B" bold="true" box="[207,459,1196,1222]" italics="true" pageId="7" pageNumber="434">Proceratophrys boiei</emphasis>
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taxonomy
</emphasis>
</heading>
</paragraph>
</subSubSection>
<subSubSection id="1BB0652CFFC98F44FF01FB50FD45FC39" lastPageId="8" lastPageNumber="435" pageId="7" pageNumber="434" type="reference_group">
<paragraph id="531536A7FFC98F4BFF01FB50FEABFA23" blockId="7.[151,1436,1266,2011]" pageId="7" pageNumber="434">
<taxonomicName id="94AA4D24FFC98F4BFF01FB50FE1EFA96" box="[151,389,1267,1291]" class="Amphibia" family="Cycloramphidae" genus="Proceratophrys" kingdom="Animalia" order="Anura" pageId="7" pageNumber="434" phylum="Chordata" rank="species" species="boiei">
<emphasis id="61DEEAB5FFC98F4BFF01FB50FE1EFA96" box="[151,389,1267,1291]" italics="true" pageId="7" pageNumber="434">Proceratophrys boiei</emphasis>
</taxonomicName>
is de most widely distributed species in the genus, occurring from southeastern Minas Gerais and Espírito Santo to southeastern Santa Catarina (
<bibRefCitation id="373B4B56FFC98F4BFD41FAB5FCC5FAB3" author="Frost" box="[727,862,1302,1326]" pageId="7" pageNumber="434" refString="Frost, D. R. (2013). Amphibian Species of the World: an Online Reference. Version 5.6. American Museum of Natural History, New York, USA. Available from: http: // research. amnh. org / herpetology / amphibia / index. html. (accessed 15 February 2013)" type="journal article" year="2013">Frost, 2013</bibRefCitation>
). 
<bibRefCitation id="373B4B56FFC98F4BFCE4FAB5FB1AFAB3" author="Prado" box="[882,1153,1302,1326]" pageId="7" pageNumber="434" refString="Prado, G. M &amp; Pombal, J. P. (2008) Especies de Proceratophrys Miranda-Ribeiro, 1920 com apendices palpebrais (Anura; Cycloramphidae). Arquivos de Zoologia, 39, 1 - 85." type="journal article" year="2008">Prado &amp; Pombal (2008)</bibRefCitation>
revised the taxonomy of this species, and did not find morphometric differences among the samples from different localities along the species distributions. However, they mentioned a tendency of decreasing of the curvature of frontoparietals crests and an increase in the prominence of the posterior portion of the same feature in specimens of Santa Catarina and Paraná states.
</paragraph>
<paragraph id="531536A7FFC98F4BFF51FA69FDA9F9B6" blockId="7.[151,1436,1266,2011]" pageId="7" pageNumber="434">
<bibRefCitation id="373B4B56FFC98F4BFF51FA69FE49FA7F" author="Prado" box="[199,466,1482,1506]" pageId="7" pageNumber="434" refString="Prado, G. M &amp; Pombal, J. P. (2008) Especies de Proceratophrys Miranda-Ribeiro, 1920 com apendices palpebrais (Anura; Cycloramphidae). Arquivos de Zoologia, 39, 1 - 85." type="journal article" year="2008">Prado &amp; Pombal (2008)</bibRefCitation>
also noted a marked depth on the head in specimens of Rio de Janeiro. They opted not to give specific status to those populations because they found great variation in those characters along the distribution of 
<emphasis id="61DEEAB5FFC98F4BFEABF9B0FDA9F9B6" box="[317,562,1555,1579]" italics="true" pageId="7" pageNumber="434">
<taxonomicName id="94AA4D24FFC98F4BFEABF9B0FDB5F9B6" box="[317,558,1555,1579]" class="Amphibia" family="Cycloramphidae" genus="Proceratophrys" kingdom="Animalia" order="Anura" pageId="7" pageNumber="434" phylum="Chordata" rank="species" species="boiei">Proceratophrys boiei</taxonomicName>
.
</emphasis>
</paragraph>
<paragraph id="531536A7FFC98F4BFF51F994FB6FF927" blockId="7.[151,1436,1266,2011]" pageId="7" pageNumber="434">
More recently, Amaro 
<emphasis id="61DEEAB5FFC98F4BFE5FF99BFE67F9D3" box="[457,508,1590,1615]" italics="true" pageId="7" pageNumber="434">et al</emphasis>
. (2012) investigated the demographic history of 
<taxonomicName id="94AA4D24FFC98F4BFBBEF995FA8CF9D3" box="[1064,1303,1590,1614]" class="Amphibia" family="Cycloramphidae" genus="Proceratophrys" kingdom="Animalia" order="Anura" pageId="7" pageNumber="434" phylum="Chordata" rank="species" species="boiei">
<emphasis id="61DEEAB5FFC98F4BFBBEF995FA8CF9D3" box="[1064,1303,1590,1614]" italics="true" pageId="7" pageNumber="434">Proceratophrys boiei</emphasis>
</taxonomicName>
using three molecular markers (RAG-1; Cytb; 16S) and chromosomal data. They found two well supported clade, which they called South clade, including specimens from the southeastern São Paulo and Santa Catarina, and North clade, including specimens from northeastern São Paulo, Rio de Janeiro, Minas Gerais and Espírito Santo.
</paragraph>
<paragraph id="531536A7FFC98F4BFF51F965FD95F8D7" blockId="7.[151,1436,1266,2011]" pageId="7" pageNumber="434">
They also found a strongly supported division of the North clade in two; the North clade 1 for the specimens from Espírito Santo and Minas Gerais, and the North clade 2 for Rio de Janeiro and São Paulo. They emphasized the need of examination of additional morphological and acoustic characters to reveal phenotypic congruence with their results (Amaro 
<emphasis id="61DEEAB5FFC98F4BFEE9F897FE23F8D6" box="[383,440,1843,1867]" italics="true" pageId="7" pageNumber="434">et al.</emphasis>
, 2012).
</paragraph>
<paragraph id="531536A7FFC98F4BFF51F8F4FD28F847" blockId="7.[151,1436,1266,2011]" pageId="7" pageNumber="434">
We found a significant morphological variation in the chondrocranium of the three populations of 
<taxonomicName id="94AA4D24FFC98F4BFF01F8D8FE17F80E" box="[151,396,1915,1939]" class="Amphibia" family="Cycloramphidae" genus="Proceratophrys" kingdom="Animalia" order="Anura" pageId="7" pageNumber="434" phylum="Chordata" rank="species" species="boiei">
<emphasis id="61DEEAB5FFC98F4BFF01F8D8FE17F80E" box="[151,396,1915,1939]" italics="true" pageId="7" pageNumber="434">Proceratophrys boiei</emphasis>
</taxonomicName>
studied. The population of Rio de Janeiro state, represented by tadpoles collected in Teresópolis municipality, is more similar to the other species of 
<taxonomicName id="94AA4D24FFC98F4BFCF9F83DFB86F82B" box="[879,1053,1950,1974]" class="Amphibia" family="Cycloramphidae" genus="Proceratophrys" kingdom="Animalia" order="Anura" pageId="7" pageNumber="434" phylum="Chordata" rank="genus">
<emphasis id="61DEEAB5FFC98F4BFCF9F83DFB86F82B" box="[879,1053,1950,1974]" italics="true" pageId="7" pageNumber="434">Proceratophrys</emphasis>
</taxonomicName>
that possess palpebral appendage (
<taxonomicName id="94AA4D24FFC98F4BFF36F867FEC7F846" box="[160,348,1987,2011]" class="Amphibia" family="Cycloramphidae" genus="Proceratophrys" kingdom="Animalia" order="Anura" pageId="7" pageNumber="434" phylum="Chordata" rank="species" species="appendiculata">
<emphasis id="61DEEAB5FFC98F4BFF36F867FEC7F846" box="[160,348,1987,2011]" italics="true" pageId="7" pageNumber="434">P. appendiculata</emphasis>
</taxonomicName>
, 
<taxonomicName id="94AA4D24FFC98F4BFEFCF867FE47F846" box="[362,476,1987,2011]" class="Amphibia" family="Cycloramphidae" genus="Proceratophrys" kingdom="Animalia" order="Anura" pageId="7" pageNumber="434" phylum="Chordata" rank="species" species="laticeps">
<emphasis id="61DEEAB5FFC98F4BFEFCF867FE47F846" box="[362,476,1987,2011]" italics="true" pageId="7" pageNumber="434">P. laticeps</emphasis>
</taxonomicName>
and 
<taxonomicName id="94AA4D24FFC98F4BFD85F867FD38F846" box="[531,675,1987,2011]" class="Amphibia" family="Cycloramphidae" genus="Proceratophrys" kingdom="Animalia" order="Anura" pageId="7" pageNumber="434" phylum="Chordata" rank="species" species="tupinamba">
<emphasis id="61DEEAB5FFC98F4BFD85F867FD38F846" box="[531,675,1987,2011]" italics="true" pageId="7" pageNumber="434">P tupinamba</emphasis>
</taxonomicName>
).
</paragraph>
<paragraph id="531536A7FFC68F44FF51FF34FB23FEA2" blockId="8.[151,1436,151,932]" pageId="8" pageNumber="435">
Specimens from Minas Gerais presented elongations of the taenia tecti marginales and of the tectum synoticum, originating the taenia tecti medialis and transversales. It has been shown that this might occur along the development of the chondrocranium (
<bibRefCitation id="373B4B56FFC68F44FDD5FF7CFCB0FF6A" author="Candioti" box="[579,811,223,248]" pageId="8" pageNumber="435" refString="Candioti, M. F. V., Ubeda, C. &amp; Lavilla, E. O. (2005) Morphology and metamorphosis of Eupsophus calcaratus tadpoles (Anura: Leptodactylidae). Journal of Morphology, 262, 161 - 177. http: // dx. doi. org / 10.1002 / jmor. 10320" type="journal article" year="2005">
Candioti 
<emphasis id="61DEEAB5FFC68F44FD38FF42FD73FF65" box="[686,744,224,248]" italics="true" pageId="8" pageNumber="435">et al.</emphasis>
2005
</bibRefCitation>
) but it does not seem to be the case. Specimens of the same developmental stages of others populations and ontogenetic series of others species did not show such variations, leading us to conclude that it is a particularity of the specimens from Minas Gerais.
</paragraph>
<paragraph id="531536A7FFC68F44FF51FEEFFBA2FE1A" blockId="8.[151,1436,151,932]" pageId="8" pageNumber="435">The morphology of the suprarostral cartilage also corroborates this hypothesis. The cartilaginous connection of the distal portion of the alae with the corpora was only observed in this population.</paragraph>
<paragraph id="531536A7FFC68F44FF51FE37FD13FD8A" blockId="8.[151,1436,151,932]" pageId="8" pageNumber="435">
The population of Paraná state also presented unique morphology. The hipobranchial planum is reduced and ends in a rounded projection. The ceratobranchial IV is clearly more developed and the pars reuniens is expanded in midline. Our data is congruent with the pattern recovered by Amaro 
<emphasis id="61DEEAB5FFC68F44FB85FE7EFBD5FE69" box="[1043,1102,476,500]" italics="true" pageId="8" pageNumber="435">et al</emphasis>
. (2012), with morphotypes representing the three clades found by them.
</paragraph>
<paragraph id="531536A7FFC68F44FF51FD87FC55FD51" blockId="8.[151,1436,151,932]" pageId="8" pageNumber="435">
The genus 
<taxonomicName id="94AA4D24FFC68F44FED3FD87FE6FFDA1" box="[325,500,548,572]" class="Amphibia" family="Cycloramphidae" genus="Proceratophrys" kingdom="Animalia" order="Anura" pageId="8" pageNumber="435" phylum="Chordata" rank="genus">
<emphasis id="61DEEAB5FFC68F44FED3FD87FE6FFDA1" box="[325,500,548,572]" italics="true" pageId="8" pageNumber="435">Proceratophrys</emphasis>
</taxonomicName>
has been shown more diverse than previously thought—eleven new species were described in the last five years (
<bibRefCitation id="373B4B56FFC68F44FE6DFDE4FD61FDC2" author="Prado" box="[507,762,583,607]" pageId="8" pageNumber="435" refString="Prado, G. M &amp; Pombal, J. P. (2008) Especies de Proceratophrys Miranda-Ribeiro, 1920 com apendices palpebrais (Anura; Cycloramphidae). Arquivos de Zoologia, 39, 1 - 85." type="journal article" year="2008">Prado &amp; Pombal 2008</bibRefCitation>
; 
<bibRefCitation id="373B4B56FFC68F44FC90FDE4FC74FDC2" author="Cruz" box="[774,1007,583,607]" pageId="8" pageNumber="435" refString="Cruz, C. A. G. &amp; Napoli, M. F. (2010) A new species of smooth horned frog, genus Proceratophrys Miranda-Ribeiro (Amphibia: Anura: Cycloramphidae), from the Atlantic Rain Forest eastern Bahia, Brazil, Zootaxa, 1660, 57 - 67." type="journal article" year="2010">Cruz &amp; Napoli 2010</bibRefCitation>
; 
<bibRefCitation id="373B4B56FFC68F44FC6DFDE4FB21FDC2" author="Avila" box="[1019,1210,583,608]" pageId="8" pageNumber="435" refString="Avila, R. W., Kawashita-Ribeiro, R. A. &amp; Morais, D. H. (2011) A new species of Proceratophrys (Anura: Cycloramphidae) from western Brazil. Zootaxa, 2890, 20 - 28." type="journal article" year="2011">
Ávila 
<emphasis id="61DEEAB5FFC68F44FBD7FDEAFBE9FDFD" box="[1089,1138,584,608]" italics="true" pageId="8" pageNumber="435">et al</emphasis>
. 2011
</bibRefCitation>
; 
<bibRefCitation id="373B4B56FFC68F44FB50FDE4FF4AFD19" author="Martins" pageId="8" pageNumber="435" refString="Martins, L. B. &amp; Giaretta, A. A. (2011) A new species of Proceratophrys Miranda-Ribeiro (Amphibia: Anura: Cycloramphidae) from central Brazil. Zootaxa, 2880, 41 - 50." type="journal article" year="2011">Martins &amp; Giaretta 2011</bibRefCitation>
; 
<bibRefCitation id="373B4B56FFC68F44FF76FDCFFE2DFD19" author="Napoli" box="[224,438,620,644]" pageId="8" pageNumber="435" refString="Napoli, M. F., Cruz, C. A. G., Abreu, R. O. &amp; Del-Grande, M. L. (2011) A new species of Proceratophrys Miranda-Ribeiro (Amphibia: Anura: Cycloramphidae) from the Chapada Diamantina, State of Bahia, northeastern Brazil. Zootaxa, 3133, 37 - 49." type="journal article" year="2011">
Napoli 
<emphasis id="61DEEAB5FFC68F44FEA0FDCEFEF0FD19" box="[310,363,620,644]" italics="true" pageId="8" pageNumber="435">et al</emphasis>
. 2011
</bibRefCitation>
; 
<bibRefCitation id="373B4B56FFC68F44FE53FDCFFD1DFD19" author="Cruz" box="[453,646,620,644]" pageId="8" pageNumber="435" refString="Cruz, C. A. G., Nunes, I. &amp; Junca, F. A. (2012) Redescription of Proceratophrys cristiceps (Muller, 1883) (Amphibia, Anura, Cycloramphidae), with description of two new species without eyelid appendages from northeastern Brazil. South America Journal of Herpetology, 7, 110 - 122. http: // dx. doi. org / 10.2994 / 057.007.0201" type="journal article" year="2012">
Cruz 
<emphasis id="61DEEAB5FFC68F44FD93FDCEFDA1FD19" box="[517,570,620,644]" italics="true" pageId="8" pageNumber="435">et al</emphasis>
. 2012
</bibRefCitation>
; 
<bibRefCitation id="373B4B56FFC68F44FD03FDCFFCE0FD19" author="Teixeira" box="[661,891,620,644]" pageId="8" pageNumber="435" refString="Teixeira, M., Amaro, R. C., Recoder, R. S., Dal Vechio, F. &amp; Rodrigues, M. T. (2012) A new dwarf species of Proceratophrys Miranda-Ribeiro, 1920 (Anura, Cycloramphidae) from highlands of Chapada Diamantina, Bahia, Brazil. Zootaxa, 3551, 25 - 42." type="journal article" year="2012">
Teixeira 
<emphasis id="61DEEAB5FFC68F44FD6DFDCEFCB4FD19" box="[763,815,620,644]" italics="true" pageId="8" pageNumber="435">et al</emphasis>
. 2012
</bibRefCitation>
; 
<bibRefCitation id="373B4B56FFC68F44FC1CFDCFFBD1FD19" author="Dias" box="[906,1098,620,644]" pageId="8" pageNumber="435" refString="Dias, P. H. S., Amaro, R. C., Carvalho-e-Silva, A. M. P. &amp; Rodrigues, M. T. (2013) Two new species of Proceratophrys Miranda- Ribeiro, 1920 (Anura; Odontophrynidae) from Atlantic Forest, with taxonomic remarks on the genus. Zootaxa, 3682, 277 - 304. http: // dx. doi. org / 10.11646 / zootaxa. 3682.2.5" type="journal article" year="2013">
Dias 
<emphasis id="61DEEAB5FFC68F44FC5EFDCEFC67FD19" box="[968,1020,620,644]" italics="true" pageId="8" pageNumber="435">et al</emphasis>
. 2013
</bibRefCitation>
). Moreover, the geographical distributions of the species are highly vicariant (
<bibRefCitation id="373B4B56FFC68F44FD38FD2CFC04FD3A" author="Izecksohn" box="[686,927,655,680]" pageId="8" pageNumber="435" refString="Izecksohn, E., Cruz, C. A. G. &amp; Peixoto, O. L. (1998) Sobre Proceratophrys appendiculata e algumas especies afins (Amphibia: Anura: Leptodactylidae). Revista da Universidade Rural, Serie Ciencias da Vida, 20, 37 - 54." type="journal article" year="1998">
Izecksohn 
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) with few areas of sympatry among then, and it is expected that more than one taxon exist within 
<taxonomicName id="94AA4D24FFC68F44FD4FFD17FC5CFD51" box="[729,967,692,716]" class="Amphibia" family="Cycloramphidae" genus="Proceratophrys" kingdom="Animalia" order="Anura" pageId="8" pageNumber="435" phylum="Chordata" rank="species" species="boiei">
<emphasis id="61DEEAB5FFC68F44FD4FFD17FC5CFD51" box="[729,967,692,716]" italics="true" pageId="8" pageNumber="435">Proceratophrys boiei</emphasis>
</taxonomicName>
.
</paragraph>
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In recent years taxonomists have employed an integrative approach in species descriptions, and distinct lines of evidences may be evoked to propose hypothesis of new species (
<bibRefCitation id="373B4B56FFC68F44FC11FD5FFBCCFC89" author="Padial" box="[903,1111,764,788]" pageId="8" pageNumber="435" refString="Padial, J. M., Castroviejo-Fisher, S., Kohler, J., Vila, C., Chaparro, J. C. &amp; De la Riva, I. (2009) Deciphering the products of evolution at species level: the need for a integrative taxonomy. Zoologica Scripta, 38, 431 - 447. http: // dx. doi. org / 10.1111 / j. 1463 - 6409.2008.00381. x" type="journal article" year="2009">
Padial 
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, 2010; Padial &amp; 
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la Riva 2010; 
<bibRefCitation id="373B4B56FFC68F44FF75FC82FE34FCAA" author="Rosa" box="[227,431,799,824]" pageId="8" pageNumber="435" refString="Rosa, G. M., Andreone, F., Crottini, A., Hauswaldt, J. S., Noel, J., Rabibisoa, H., Randriambahiniarime, M. O., Rebelo, R. &amp; Roxworthy, C. J. (2012) The amphibians of the relict Betampona low-elevation rainforest, eastern Madagascar: an application of the integrative taxonomy approach to biodiversity assessments. Biodivesity and Conservation, 21, 1531 - 1559. http: // dx. doi. org / 10.1007 / s 10531 - 012 - 0262 - x" type="journal article" year="2012">
Rosa 
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). Our findings on chondrocranium morphology plus the molecular and chromosomal evidences provided by Amaro 
<emphasis id="61DEEAB5FFC68F44FE6FFCE6FDB6FCC1" box="[505,557,836,860]" italics="true" pageId="8" pageNumber="435">et al</emphasis>
. (2012) lead us to propose that the populations of Minas Gerais and Paraná states might represent new evolutionary lineages and should be treated as unconfirmed candidate specie (UCS) (Vieties 
<emphasis id="61DEEAB5FFC68F44FF63FC2EFEBDFC39" box="[245,294,908,932]" italics="true" pageId="8" pageNumber="435">et al</emphasis>
. 2009) until we finish further analyses.
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