Cryptic speciation in a Holarctic passerine revealed by genetic and bioacoustic analyses
Geographical Variation in Morphological and Bioacoustic Traits of Pseudopaludicola mystacalis (Cope,...
14
Research Article Geographical Variation in Morphological and Bioacoustic Traits of Pseudopaludicola mystacalis (Cope, 1887) and a Reassessment of the Taxonomic Status of Pseudopaludicola serrana Toledo, 2010 (Anura: Leptodactylidae: Leiuperinae) André Pansonato, 1 Jessica Rhaiza Mudrek, 2 Fernanda Simioni, 1 Itamar Alves Martins, 1,3 and Christine Strüssmann 2,4 1 P´ os-Graduac ¸˜ ao em Biologia Animal, Universidade Estadual Paulista (UNESP), Rua Crist´ ov˜ ao Colombo 2265, Jardim Nazareth, 15054-000 S˜ ao Jos´ e do Rio Preto, SP, Brazil 2 P´ os-Graduac ¸˜ ao em Ecologia e Conservac ¸˜ ao da Biodiversidade, Instituto de Biociˆ encias, Universidade Federal de Mato Grosso (UFMT), Avenida Fernando Correa da Costa 2367, Boa Esperanc ¸a, 78060-900 Cuiab´ a, MT, Brazil 3 Laborat´ orio de Zoologia, Instituto B´ asico de Biociˆ encias, Universidade de Taubat´ e (UNITAU), Avenida Tiradentes 500, 12030-180 Taubat´ e, SP, Brazil 4 Departamento de Ciˆ encias B´ asicas e Produc ¸˜ ao Animal, Faculdade de Agronomia, Medicina Veterin´ aria e Zootecnia, Universidade Federal de Mato Grosso (UFMT), Avenida Fernando Correa da Costa 2367, Boa Esperanc ¸a, 78060-900 Cuiab´ a, MT, Brazil Correspondence should be addressed to Andr´ e Pansonato; [email protected] Received 4 April 2014; Revised 11 June 2014; Accepted 4 July 2014; Published 12 August 2014 Academic Editor: Ariovaldo A. Giaretta Copyright © 2014 Andr´ e Pansonato et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Comparisons of advertisement calls of anurans can be used to determine intra- and interspecific differences or affinities. Described from midwestern Brazil, Pseudopaludicola mystacalis is widely distributed and abundant in major open Brazilian ecosystems. However, researchers frequently fail to determine the true taxonomic status of some of these populations and attribute them to unidentified or misidentified species. Herein, we employ morphological and bioacoustic data to reassess the distribution range and to evaluate intraspecific variation in P. mystacalis based on specimens from fiſteen localities and seven Brazilian states. We also reassess the distribution and taxonomic status of Pseudopaludicola serrana, herein considered as a junior synonym of P. murundu based on morphology, bioacoustics, and molecular data. 1. Introduction Advertisement calls are important for mate recognition in anurans and hence contribute to premating isolation among sympatric species [1]. Comparison of advertisement calls can be used to determine differences and affinities among differ- ent anuran species and so to determine taxonomic identity and phylogenetic relationships [2, 3]. Such comparisons may be especially useful for situations in which the taxonomic identity of a species is uncertain or contested involving syn- onymies, redescriptions, and species resurrections. Indeed, in the absence of consistent morphological characters for inter- specific distinctiveness, advertisement calls have proven to be of great help in revealing and supporting hypotheses of putative new species of Pseudopaludicola [4–9]. Described from midwestern Brazil (Chapada dos Guimar˜ aes, Mato Grosso), Pseudopaludicola mystacalis is widely distributed and abundant in open environments along Hindawi Publishing Corporation Advances in Zoology Volume 2014, Article ID 563165, 13 pages http://dx.doi.org/10.1155/2014/563165
Transcript of Geographical Variation in Morphological and Bioacoustic Traits of Pseudopaludicola mystacalis (Cope,...
Research ArticleGeographical Variation in Morphologicaland Bioacoustic Traits of Pseudopaludicola mystacalis(Cope 1887) and a Reassessment of the TaxonomicStatus of Pseudopaludicola serrana Toledo 2010(Anura Leptodactylidae Leiuperinae)
Andreacute Pansonato1 Jessica Rhaiza Mudrek2 Fernanda Simioni1
Itamar Alves Martins13 and Christine Struumlssmann24
1 Pos-Graduacao em Biologia Animal Universidade Estadual Paulista (UNESP) Rua Cristovao Colombo 2265Jardim Nazareth 15054-000 Sao Jose do Rio Preto SP Brazil
2 Pos-Graduacao em Ecologia e Conservacao da Biodiversidade Instituto de BiocienciasUniversidade Federal de Mato Grosso (UFMT) Avenida Fernando Correa da Costa 2367 Boa Esperanca78060-900 Cuiaba MT Brazil
3 Laboratorio de Zoologia Instituto Basico de Biociencias Universidade de Taubate (UNITAU)Avenida Tiradentes 500 12030-180 Taubate SP Brazil
4Departamento de Ciencias Basicas e Producao Animal Faculdade de Agronomia Medicina Veterinaria e ZootecniaUniversidade Federal de Mato Grosso (UFMT) Avenida Fernando Correa da Costa 2367 Boa Esperanca78060-900 Cuiaba MT Brazil
Correspondence should be addressed to Andre Pansonato andre-panhotmailcom
Received 4 April 2014 Revised 11 June 2014 Accepted 4 July 2014 Published 12 August 2014
Academic Editor Ariovaldo A Giaretta
Copyright copy 2014 Andre Pansonato et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited
Comparisons of advertisement calls of anurans can be used to determine intra- and interspecific differences or affinities Describedfrom midwestern Brazil Pseudopaludicola mystacalis is widely distributed and abundant in major open Brazilian ecosystemsHowever researchers frequently fail to determine the true taxonomic status of some of these populations and attribute them tounidentified or misidentified species Herein we employ morphological and bioacoustic data to reassess the distribution range andto evaluate intraspecific variation in P mystacalis based on specimens from fifteen localities and seven Brazilian states We alsoreassess the distribution and taxonomic status of Pseudopaludicola serrana herein considered as a junior synonym of P murundubased on morphology bioacoustics and molecular data
1 Introduction
Advertisement calls are important for mate recognition inanurans and hence contribute to premating isolation amongsympatric species [1] Comparison of advertisement calls canbe used to determine differences and affinities among differ-ent anuran species and so to determine taxonomic identityand phylogenetic relationships [2 3] Such comparisons maybe especially useful for situations in which the taxonomic
identity of a species is uncertain or contested involving syn-onymies redescriptions and species resurrections Indeed inthe absence of consistent morphological characters for inter-specific distinctiveness advertisement calls have proven tobe of great help in revealing and supporting hypotheses ofputative new species of Pseudopaludicola [4ndash9]
Described from midwestern Brazil (Chapada dosGuimaraes Mato Grosso) Pseudopaludicola mystacalis iswidely distributed and abundant in open environments along
Hindawi Publishing CorporationAdvances in ZoologyVolume 2014 Article ID 563165 13 pageshttpdxdoiorg1011552014563165
2 Advances in Zoology
Table 1 Measurements (mm) of specimens of Pseudopaludicola mystacalis from localities in four Brazilian states Values are presented asmean plusmn standard deviation (minimumndashmaximum)119873 = number of specimens analyzed
Mato Grosso Sao Paulo Goias ParaMales Females Males Females Males Females Males
(119873 = 53) (119873 = 20) (119873 = 14) (119873 = 7) (119873 = 20) (119873 = 6) (119873 = 14)
SVL 139 plusmn 13 163 plusmn 09 139 plusmn 05 153 plusmn 07 141 plusmn 01 159 plusmn 09 154 plusmn 08
(109ndash163) (143ndash181) (13ndash149) (143ndash16) (117ndash165) (146ndash17) (146ndash166)
HL 54 plusmn 04 62 plusmn 05 54 plusmn 03 55 plusmn 03 53 plusmn 04 58 plusmn 05 56 plusmn 02
(44ndash65) (52ndash75) (46ndash59) (51ndash60) (47ndash61) (50ndash63) (53ndash59)
HW 48 plusmn 05 59 plusmn 06 48 plusmn 02 51 plusmn 04 49 plusmn 05 55 plusmn 04 48 plusmn 03
(37ndash67) (50ndash68) (43ndash51) (46ndash58) (43ndash64) (49ndash59) (45ndash53)
IOD 11 plusmn 02 14 plusmn 02 12 plusmn 01 13 plusmn 01 12 plusmn 02 14 plusmn 02 14 plusmn 02
(07ndash16) (08ndash17) (10ndash14) (11ndash14) (10ndash17) (12ndash18) (11ndash15)
ED 16 plusmn 02 17 plusmn 02 14 plusmn 01 15 plusmn 02 15 plusmn 01 16 plusmn 01 17 plusmn 008
(10ndash19) (13ndash23) (11ndash17) (13ndash19) (12ndash17) (14ndash18) (16ndash18)
END 12 plusmn 02 14 plusmn 02 11 plusmn 007 13 plusmn 02 12 plusmn 01 13 plusmn 01 12 plusmn 01
(07ndash18) (11ndash21) (10ndash12) (11ndash18) (09ndash15) (11ndash14) (11ndash14)
IND 12 plusmn 02 15 plusmn 02 13 plusmn 01 14 plusmn 009 14 plusmn 01 15 plusmn 02 13 plusmn 009
(08ndash17) (10ndash19) (11ndash15) (13ndash15) (11ndash17) (12ndash17) (12ndash14)
HAL 37 plusmn 03 44 plusmn 07 39 plusmn 02 42 plusmn 04 38 plusmn 02 41 plusmn 03 39 plusmn 02
(31ndash44) (32ndash63) (35ndash43) (38ndash48) (34ndash44) (38ndash45) (36ndash41)
THL 63 plusmn 05 77 plusmn 09 62 plusmn 03 66 plusmn 06 65 plusmn 05 74 plusmn 02 68 plusmn 02
(51ndash73) (64ndash94) (56ndash69) (53ndash71) (56ndash73) (71ndash77) (66ndash72)
TL 69 plusmn 05 83 plusmn 09 7 plusmn 03 75 plusmn 03 71 plusmn 04 78 plusmn 02 74 plusmn 02
(59ndash82) (72ndash98) (67ndash76) (71ndash78) (64ndash80) (75ndash81) (72ndash76)
TAL 39 plusmn 04 45 plusmn 06 39 plusmn 02 43 plusmn 03 39 plusmn 03 43 plusmn 03 39 plusmn 03
(31ndash46) (31ndash52) (35ndash45) (39ndash46) (32ndash45) (40ndash48) (34ndash42)
FL 77 plusmn 05 92 plusmn 08 79 plusmn 03 84 plusmn 05 77 plusmn 04 85 plusmn 06 81 plusmn 05
(63ndash92) (79ndash106) (73ndash84) (76ndash89) (69ndash82) (78ndash92) (76ndash88)
South American ldquodiagonal of open formationsrdquo [8] Howeversome populations along the speciesrsquo range are not recognizedas belonging to this taxon being rather attributed to othertaxonomic entities such as Pseudopaludicola aff falcipesPseudopaludicola aff mystacalis and Pseudopaludicola sp[10ndash14] Therefore an integrative taxonomic revision isneeded to clarify the distribution range and variation in thisspecies [9]
In spite of great morphological similarity among most ofthe 18 species of Pseudopaludicola currently recognized threeof them are readily distinguished from the others by havinglonger hindlimbs [4ndash6 8 9] Pseudopaludicola saltica (Cope1887) Pseudopaludicola murundu Toledo Siqueira DuarteVeiga-Menoncello Recco-Pimentel and Haddad 2010 andPseudopaludicola serrana Toledo 2010 Advertisement callsof all three species are similarly composed of series of noteswith nonconcatenated pulses [8 15ndash17] and they all share 2119899 =22 chromosomes [16 18] comprising a monophyletic clade[19] However the results of a recent molecular phylogeneticanalysis suggested that P serrana is a junior synonym of Pmurundu [19]
Objectives of the present article are (1) to provide andto discuss the intraspecific variation in morphological andbioacoustic traits of P mystacalis along its distribution rangein Brazil (2) to reassess the taxonomic status of P serranabased on the reinterpretation of the literature data and on theexamination of new materials (specimens and calls) freshlyobtained at the type-locality andor its vicinities of P serranaand related species
2 Material and Methods
Examined specimens of P mystacalis P murundu P salticaand P serrana (Appendices A and B) are deposited in thefollowing collections ldquoColecao Zoologica de VertebradosUniversidade Federal de Mato Grossordquo (UFMT CuiabaMato Grosso Brazil) ldquoColecao Herpetologica da Universi-dade Federal do Cearardquo (UFC Fortaleza Ceara) ldquoFonotecaNeotropical Jacques Vielliardrdquo (FNJV Campinas Sao Paulo)and ldquoMuseu de Ciencias Naturaisrdquo (MCNAM Belo Hor-izonte Minas Gerais) Material deposited at UFMT was
Advances in Zoology 3
Table 2 Measurements (mm) of the topotypes of Pseudopaludicola serrana and P murundu Values are presented as mean plusmn standarddeviation (minimumndashmaximum) Additional localities (state of Minas Gerais municipalities of Itabirito Lavras Novas Mariana OuroBranco Sao Joao Del Rei and Botumirim)119873 = number of specimens analyzed
Pseudopaludicola serrana Pseudopaludicola murunduTopotypes Additional localities Topotypes
Males Females Males Females Males Females(119873 = 5) (119873 = 1) (119873 = 16) (119873 = 5) (119873 = 5) (119873 = 1)
SVL 163 plusmn 12 177 152 plusmn 09 171 plusmn 12 159 plusmn 08 173(146ndash175) (126ndash167) (159ndash185) (152ndash169)
HL 65 plusmn 05 68 60 plusmn 04 67 plusmn 03 61 plusmn 04 68(62ndash73) (48ndash69) (63ndash71) (56ndash67)
HW 60 plusmn 02 66 55 plusmn 04 63 plusmn 03 55 plusmn 02 59(57ndash63) (47ndash61) (59ndash67) (53ndash58)
IOD 14 plusmn 01 18 14 plusmn 01 16 plusmn 007 14 plusmn 008 15(13ndash16) (12ndash16) (15ndash17) (13ndash15)
ED 16 plusmn 007 17 15 plusmn 01 16 plusmn 009 16 plusmn 02 19(15ndash17) (13ndash17) (15ndash17) (14ndash18)
END 16 plusmn 009 16 15 plusmn 01 15 plusmn 008 15 plusmn 008 16(15ndash17) (13ndash17) (14ndash16) (14ndash16)
IND 15 plusmn 01 18 14 plusmn 01 16 plusmn 008 15 plusmn 009 16(13ndash17) (12ndash17) (15ndash17) (14ndash17)
HAL 44 plusmn 01 49 41 plusmn 04 45 plusmn 01 43 plusmn 02 49(43ndash46) (34ndash46) (43ndash47) (42ndash46)
THL 90 plusmn 03 102 85 plusmn 07 94 plusmn 05 89 plusmn 03 95(85ndash93) (68ndash94) (87ndash101) (86ndash93)
TL 109 plusmn 03 127 107 plusmn 07 118 plusmn 05 112 plusmn 03 123(106ndash113) (89ndash115) (109ndash122) (108ndash116)
TAL 53 plusmn 02 58 51 plusmn 04 57 plusmn 04 54 plusmn 007 63(51ndash57) (42ndash55) (50ndash61) (54ndash56)
FL 98 plusmn 03 111 93 plusmn 08 102 plusmn 05 106 plusmn 04 114(95ndash103) (74ndash104) (95ndash106) (99ndash109)
collected with permission of the ldquoInstituto Chico Mendes deConservacao da Biodiversidaderdquo (ICMBIO 27231-1)
Since the available diagnoses for P serrana and Pmurundu do not allow clearly distinguishing specimens fromthese two species newmaterial from additional localities wasputatively associated with each of them based solely on thepositioning of collecting andor recording sites populationsfrom easternmost localities in Minas Gerais were consideredto represent P serrana and populations from westernmostlocalities in Minas Gerais (and those from the state of SaoPaulo) were considered to represent P murundu
The measurements of 218 adult specimens (Tables 1 and2) of P murundu (6 males 1 female) P mystacalis (101 males37 females) P saltica (39 males 3 females original data inPansonato et al [8]) and P serrana (22 males 6 females)were taken with a digital caliper to the nearest 01mmMeasurements for hand length (HAL) tibia length (TL)tarsus length (TAL) and foot length (FL) followedHeyer et al[20] Measurements for snout-vent length (SVL) head length(HL) head width (HW) interorbital distance (IOD) eye
diameter (ED) eye-nostril distance (END) internarial dis-tance (IND) and thigh length (THL) followedDuellman [21]
Vocalizations of specimens of Pmurundu Pmystacalis Psaltica andP serranawere recorded byAndre Pansonatowitha professional digital recorder Marantz PMD 660 equippedwith a Yoga EM-9600 external directional microphoneDigital recordings were sampled at 441 kHz sampling rateand 16 bit resolution and saved in uncompressed wave filesSpectrograms were edited using Raven Pro 13 software withthe following configuration for P mystacalis brightness 75contrast 80 DFT size 512 samples 3 dB filter bandwidth112Hz time grid overlap 50 forPmurunduP saltica andPserrana brightness 70 contrast 80 DFT size 512 samples3 dB filter bandwidth 124Hz time grid overlap 50
We analyzed 1894 notes (Tables 3 and 4) 503 from Pmurundu 444 notes from P mystacalis 577 from P salticaand 370 from P serrana The following temporal variableswere measured from the waveform number of pulses pernote note and pulse duration (ms) internote and interpulseinterval (ms) Note that repetition rate was calculated in
4 Advances in Zoology
Table 3 Measurements of bioacoustic variables of the advertisement calls of specimens of Pseudopaludicola mystacalis from 12 localities inseven Brazilian states (CE Ceara GO Goias MA Maranhao MT Mato Grosso PA Para PI Piauı SP Sao Paulo) Values are presented asmean plusmn standard deviation (minimumndashmaximum)119873 number of notes analyzed
LocalitymdashState Air temp Noteduration (ms)
Internoteinterval (ms)
Pulses pernote
Pulseduration (ms)
Dominantfrequency (Hz)
Notesmin(mean)
PoconemdashMT (119873 = 30) 256∘C 40 plusmn 5
(30ndash50)80 plusmn 10
(60ndash100)16 plusmn 12
(14ndash18)2 plusmn 03
(1-2)46842 plusmn 1157
(4522ndash49096)5111
NS LivramentomdashMT (119873 = 25) 252∘C 40 plusmn 4
(40ndash50)70 plusmn 30
(50ndash200)17 plusmn 10
(14ndash19)2 plusmn 03
(1-2)48114 plusmn 563
(47373ndash49096)5064
C GuimaraesmdashMT (119873 = 110) 263∘C 40 plusmn 4
(30ndash50)60 plusmn 10
(40ndash100)16 plusmn 08
(14ndash17)2 plusmn 04
(1-2)49624 plusmn 1815
(46512ndash52541)5769
CuiabamdashMT (119873 = 25) 26∘C 50 plusmn 4
(30ndash50)90 plusmn 10
(60ndash100)14 plusmn 08
(12ndash16)2 plusmn 04
(1ndash3)47752 plusmn 828
(46512ndash49096)4433
CuiabamdashMT (119873 = 25) 26∘C 45 plusmn 4
(30ndash50)80 plusmn 30
(50ndash200)16 plusmn 10
(13ndash18)2 plusmn 03
(1-2)48372 plusmn 150
(44789ndash49957)5243
CaceresmdashMT (119873 = 25) 26∘C 50 plusmn 3
(40ndash50)60 plusmn 50
(50ndash70)16 plusmn 10
(14ndash18)2 plusmn 03
(1-2)4901 plusmn 512
(47373ndash49957)5389
BalsasmdashMA (119873 = 30) 265∘C 40 plusmn 2
(37ndash45)80 plusmn 5
(70ndash90)16 plusmn 10
(14ndash18)2 plusmn 04
(1-2)507609 plusmn 20568
(47804ndash53402)5137
IcemmdashSP (119873 = 28) 23∘C 50 plusmn 5
(50ndash60)110 plusmn 7
(100ndash150)17 plusmn 17
(14ndash20)2 plusmn 04
(1-2)48722 plusmn 799
(47373ndash49742)3633
ItapipocamdashCE (119873 = 30) mdash 50 plusmn 3
(40ndash50)90 plusmn 10
(70ndash130)16 plusmn 12
(14ndash18)2 plusmn 04
(1-2)51282 plusmn 981
(47804ndash5211)4207
TaıbamdashCE (119873 = 30) mdash 40 plusmn 2
(40ndash50)70 plusmn 2
(60ndash70)16plusmn11(13ndash18)
2plusmn05(1ndash3)
47952plusmn852(46942ndash49526)
5353
Brejo do BuritimdashPI (119873 = 30) 27∘C 50 plusmn 1
(45ndash50)90 plusmn 20
(60ndash140)19 plusmn 06
(18ndash20) 2 486075 plusmn 3148
(48234ndash49096)4296
PrimaveramdashPA (119873 = 30) 255∘C 50 plusmn 2
(40ndash50)80 plusmn 5
(70ndash100)18plusmn12(16ndash20)
2plusmn05(1-2)
50406plusmn456(49219ndash51094)
4637
UruacumdashGO (119873 = 26) 245∘C 50plusmn2(40ndash50)
60plusmn5(50ndash80)
16plusmn12(14ndash18)
2 plusmn 05
(1-2)46334 plusmn 866
(4500ndash49688)5435
Mean plusmn SD 50 plusmn 4(30ndash60)
80 plusmn 10(40ndash200)
16 plusmn 17(12ndash20)
2 plusmn 04(1ndash3)
48874 plusmn 1495(44789ndash53402)
4901plusmn611(3633ndash5769)
notes perminute Dominant frequency (note peak frequencyHz) was obtained from the spectrogram Terminology forbioacoustic variables follows Magalhaes et al [7] Pansonatoet al [8] and Heyer et al [20] Vocalizations are archivedin the ldquoBanco de Registros Bioacusticosrdquo and housed at theldquoLaboratorio de Herpetologia do Instituto de Biociencias daUniversidade Federal de Mato Grossordquo (LH Cuiaba MatoGrosso)
Discriminant function analyses (DFA) were conducted inorder to evidence the set of morphometric and bioacousticvariables that mostly distinguish between the species ofPseudopaludicola compared herein DFA were performed oncorrelation matrices from 12 log-transformed morphometricand six bioacoustic variables using R platform version 301[22] Bioacoustic comparisons through the DFA were per-formed using mean individual values
3 Results
31 Geographical Variation in Pseudopaludicola mystacalis(Cope 1887) Based on morphology and bioacoustics Pseu-dopaludicola mystacalis was positively identified in fifteenlocalities (Figure 1) from seven Brazilian states Ceara Goias
Maranhao Mato Grosso Para Piauı and Sao Paulo Theadvertisement calls of Pseudopaludicola mystacalis along itsdistribution range in Brazil (Figures 1 and 2) consistedof series composed of 9ndash229 notes with 16 plusmn 17 (12ndash20)concatenated pulses (ie no interpulse intervals) Mean noterepetition rate was 4901 plusmn 611 notesmin (3633ndash5769)mean duration of each note was 50 plusmn 4ms (30ndash60) averageinternote interval varied from 80 plusmn 10ms (40ndash200) Meanpulse duration was 2 plusmn 04ms (1ndash3) Frequency ranged from26862Hz to 73433Hz and dominant frequency ranged from44789 to 53402Hz (Table 3)
Discriminant function analysis (DFA) with our dataon P mystacalis did not group localities neither regardingmorphometric characters (males and females) nor regardingbioacoustic variables The first function (DF1) of DFA withmorphometric data explained 63 of the variation amongmales of different populations (Figure 3(a)) and higherloadings corresponded to thigh length (105) hand length(98) and foot length (84) The DF1 explained 85 of thevariation among females (Figure 3(b)) and higher loadingscorresponded to hand length (123) foot length (107) andsnout-vent length (88) The DF1 of DFA with bioacousticvariables explained 79 of the total variation in our sample
Advances in Zoology 5
Table4
Measurementsof
bioacoustic
varia
bles
oftheadvertise
mentc
allsof
specim
enso
fPseud
opalud
icola
murun
duPsalticaandPserranaVa
lues
arepresentedas
meanplusmnsta
ndard
deviation(m
inim
umndashm
axim
um)
Species
(vou
cher
record)
Noted
uration(m
s)Internoteinterval(ms)
Pulse
duratio
n(m
s)Interpulsesinterval(ms)
Dom
inantfrequ
ency
(Hz)
Pulse
sno
teNotesm
inMun
icipality
state
Pmurun
du(LH676)
80plusmn12(58ndash105)
100plusmn15(69ndash
141)
8plusmn2(4ndash12)
26plusmn7(7ndash4
0)56007plusmn2043(5168ndash5857)33plusmn07(2ndash5)3489plusmn219(3145ndash3704)
RioClaroSP
Pmurun
du(LH677)
94plusmn11(49ndash
114)
98plusmn16(70ndash
140)
13plusmn2(9ndash17)
23plusmn9(6ndash39)
55799plusmn1502(52541ndash5857)29plusmn02(2-3)3172plusmn176(2956ndash3419)
RioClaroSP
Pmurun
du(LH678)
89plusmn13(33ndash104)
107plusmn12(89ndash
137)
9plusmn2(5ndash17)
20plusmn8(8ndash4
6)57259plusmn1297(53402ndash59001)37plusmn05(2ndash4
)3087plusmn139(2926ndash3264)
RioClaroSP
Pmurun
du(FNJV
12976)
81plusmn15(56ndash
103)
152plusmn50(79ndash
247)
9plusmn2(5ndash14)
18plusmn5(10ndash
29)
57557plusmn3226(5168ndash62016)37plusmn04(3-4)
2803
RioClaroSP
Pmurun
du(FNJV
4575)
81plusmn13(54ndash
105)
132plusmn20(97ndash193)
10plusmn2(5ndash16)
23plusmn9(5ndash50)
55755plusmn1493(4875ndash58125)34plusmn07(2ndash5)2843plusmn313(2182ndash3691)
SaoRo
qued
eMinasM
GPmurun
du(FNJV
4576)
118plusmn18(77ndash143)
159plusmn14(129ndash194)
13plusmn2(8ndash18)
27plusmn9(10ndash
54)
54603plusmn766(5250ndash
5625)36plusmn05(2ndash4
)2183plusmn198(1893ndash266
6)
Pocosd
eCaldasMG
Pserran
a(LH673)
98plusmn12(65ndash131)
184plusmn18(131ndash224)
12plusmn2(8ndash18)
16plusmn5(6ndash32)
56556plusmn1202(5168ndash5814)41plusmn03(3ndash5)2183plusmn74(2061ndash
2258)
Brum
adinho
MG
Pserran
a(LH674)
91plusmn14(49ndash
117)236plusmn25(184ndash288)
12plusmn2(6ndash17)
25plusmn8(5ndash4
1)53402plusmn293(5168ndash55125)29plusmn04(2ndash4
)1795plusmn84(1709ndash1877)
Brum
adinho
MG
Pserran
a(LH675)
83plusmn15(49ndash
99)
161plusmn51(81ndash197)
10plusmn2(7ndash16)
16plusmn7(5ndash33)
5857
37plusmn04(3-4)2494plusmn223(2282ndash2727)
SaoJoao
DelRe
iMG
Pserran
a(FNJV
12879)
60plusmn6(47ndash72)
86plusmn8(63ndash101)
8plusmn2(4ndash14)
8plusmn2(4ndash16)
57070plusmn1155(55125ndash5857)39plusmn03(3-4)4119plusmn237(3614ndash4
762)
SaoJoao
DelRe
iMG
Pserran
a(FNJV
12880)
63plusmn13(26ndash
97)
112plusmn20(75ndash166)
5plusmn1(1ndash
9)13plusmn5(4ndash33)
57737plusmn1693(55125ndash60293)38plusmn05(2ndash5)3487plusmn473(2511ndash
5172
)SaoJoao
DelRe
iMG
Psaltica
(13A
-01)
65plusmn9(48ndash86)
120plusmn19(75ndash170)
9plusmn2(5ndash13)
35plusmn14(5ndash55)
47510plusmn1042(460
81ndash49526)25plusmn05(2-3)3839plusmn36(3424ndash4
062)
Chapadad
osGuimaraesMT
Psaltica
(42A
-06)
58plusmn6(46ndash
70)
109plusmn14(90ndash
137)
8plusmn1(4ndash11)
15plusmn7(5ndash30)
49143plusmn353(48234ndash
49526)32plusmn03(3-4)3654plusmn419(2985ndash4
412)
Pontes
eLacerdaM
TPsaltica
(42A
-07)
66plusmn13(48ndash87)
186plusmn23(14
4ndash224)
11plusmn4(4ndash19)
36plusmn5(30ndash
46)
45004plusmn3398(40052ndash49526)22plusmn04(2-3)2393plusmn182(2135ndash283)
Pontes
eLacerdaM
TPsaltica
(LH12)
77plusmn8(63ndash95)
113plusmn18(80ndash
172)
6plusmn1(4ndash9
)21plusmn18(3ndash4
9)50230plusmn1357(48665ndash55125)39plusmn04(3ndash5)3183plusmn328(2299ndash3947)
PortoEstre
laM
TPsaltica
(LH13)
97plusmn6(85ndash106)
127plusmn10(99ndash
158)
5plusmn1(3ndash7)
18plusmn17(2ndash56)
52368plusmn615(50818
ndash52972
)5plusmn01(5ndash6
)2687plusmn147(2308ndash3141)
PortoEstre
laM
TPsaltica
(LH14)
78plusmn5(70ndash
92)
134plusmn17(107ndash210)
17plusmn13(4ndash4
4)6plusmn2(4ndash10)
48062plusmn677(46512
ndash49957)21plusmn03(2-3)2837plusmn253(2062ndash3389)
PortoEstre
laM
TPsaltica
(LH16)
97plusmn10(64ndash
118)
127plusmn18(93ndash162)
10plusmn3(6ndash18)
23plusmn17(3ndash56)
50359plusmn2998(43066ndash
5340
2)45plusmn06(3ndash5)2712plusmn265(2264ndash3352)
PortoEstre
laM
TPsaltica
(LH17)
73plusmn26(33ndash122)
106plusmn24(79ndash
228)
7plusmn1(4ndash8)
19plusmn13(5ndash54)
48837plusmn2099(44789ndash
5168)34plusmn05(3ndash5)3524plusmn776(2113ndash4
838)
PortoEstre
laM
TPsaltica
(LH18)
83plusmn4(75ndash100)
143plusmn17(100ndash212)
5plusmn2(3ndash16)
18plusmn14(3ndash4
7)52483plusmn443(50818
ndash52972
)41plusmn03(4-5)2670plusmn214(1987ndash
3389)
PortoEstre
laM
TPsaltica
(LH709)
86plusmn14(51ndash117
)122plusmn55(58ndash383)
6plusmn1(3ndash10)
11plusmn8(3ndash33)
51139plusmn1169(49967ndash5340
2)44plusmn05(4-5)3067plusmn725(1266ndash4
838)
Uberla
ndiaM
G
6 Advances in Zoology
60∘W 50
∘W 40∘W
0∘
10∘S
20∘S
30∘S
0 400
(km)
PA MA
PICE
4
5
6
MT
32
1
1
7
8
910
11
12
SP
GO
N
Figure 1 Geographical variation in the advertisement calls (oscillograms) of Pseudopaludicola mystacalis from twelve localities in sevenBrazilian states Para (PA) Primavera (1) Ceara (CE) Itapipoca (2) Taıba (3)Maranhao (MA) Balsas (4) Piauı (PI) Brejo do Piauı (5) Goias(GO) Uruacu (6) Mato Grosso (MT) Cuiaba (7) Chapada dos Guimaraes (8) Nossa Senhora do Livramento (9) Pocone (10) Caceres (11)Sao Paulo (SP) Icem (12) Total time of each oscillogram corresponds to 02 s
(Figure 3(c)) and higher loadings corresponded to note rate(385) internote interval (295) and note duration (221) Nodistinct groups were formed along the first function axis ofthe DFA
32 Taxonomic Status of Pseudopaludicola serrana Toledo2010 Advertisement calls of Pseudopaludicola serranarecorded at the type-locality (Brumadinho Minas Gerais)and nearly 120 km southwestwards at Serra do LenheiroMinas Gerais were similar to those of topotypes of P
murundu and distinct from topotypes of P saltica bothin spectral and temporal parameters (Figures 4 and 5)The intraspecific variation in bioacoustic parameters ofP murundu and P serrana presented below is based oncalls from topotypical specimens and on calls recorded inadditional localities listed in Appendix B
Advertisement calls of P serranawere composed of seriesof pulsed notes with nonconcatenated pulses Each note con-sisted of 36plusmn06 (range 2ndash5) pulses Mean note duration was82 plusmn 58ms (26ndash131) emitted on average at intervals of 167 plusmn58ms (63ndash288) Mean duration of each pulse was 9 plusmn 3ms
Advances in Zoology 7
Taiba(CE)
Uruaccedilu(GO)
BBuriti(PI)
C aceres
Livramento (MT)(MT)
(MT)(MT)
(MT) Pocon eCGuimaraes
Cuiab a Itapipoca(CE)
Primavera(PA)
Ic em(SP) Balsas
(MA)
(kH
z)8
7
6
5
4
3
2
1
(s)02 04 06 08 1 12 14 16 18 2 22 24 26 28 3 32 34 36 38
ı
Figure 2 Spectrograms (DFT size = 512 samples) of the advertisement calls of Pseudopaludicola mystacalis from twelve localities (two notesfor each locality) in seven Brazilian states (CE Ceara GO Goias MA Maranhao MT Mato Grosso PA Para PI Piauı SP Sao Paulo)
(2ndash18) Interpulse intervals were 16 plusmn 7ms long (4ndash41) Meanfrequency ranged from 40196 plusmn 453Hz to 70986 plusmn 312Hzand mean dominant frequency was 56251 plusmn 212Hz (5168ndash60293) Advertisement calls of Pmurunduwere composed ofseries of pulsed noteswith nonconcatenated pulses Each noteconsisted of 34 plusmn 06 (range 2ndash5) pulses Mean note durationwas 92 plusmn 18ms (33ndash143) emitted on average at intervals of121 plusmn 30ms (69ndash247) Mean duration of each pulse was 10 plusmn3ms (4ndash18) Interpulse intervals were 24plusmn8ms (5ndash54) Meanfrequency ranged from 36285 plusmn 513Hz to 73301 plusmn 355Hzand mean dominant frequency was 55901 plusmn 176Hz (4875ndash62016Hz)
A discriminant function analysis (DFA)withmorphome-tric data revealed that P serrana and P murundu overlappedalong the first function (DF1) ofDFAwhich explained 98ofthe total variation (Figure 6(a)) While the DFA did not sep-arate P serrana from P murundu both were separated froma third species (Pseudopaludicola saltica) whose individualsalso have long hindlimbs Higher loadings corresponded toeye diameter (121) tarsus length (75) and tibia length (46)DFA from bioacoustic data also separated Pseudopaludicolasaltica from P murundu and P serrana (Figure 6(b))The firstfunction (DF1) of DFA explained 99 of the total variationand higher loadings corresponded to dominant frequency(641) and number of pulses per note (61)
DFAofmorphometricmeasurements using all specimensassigned 100 of the individuals of Pseudopaludicola saltica86 of the individuals of P serrana and only 16 of theindividuals of P murundu to the correct species (Table 5)DFA of bioacoustic variables using all recorded males cor-rectly assigned 89 of the specimens of P saltica 83 of thespecimens of P murundu and 40 of P serrana (Table 5) Incontrast DFA with both morphometric and bioacoustic datausing specimens ofP saltica and amixed sample of specimensattributable to either P murundu or P serrana assigned 100of these latter to a single taxon
The overall similarity in morphology and general struc-ture of the call of P murundu and P serrana evidenced bythe results of DFA with 12 morphometric and six bioacous-tic variables strongly support the rejection of the specificstatus of Pseudopaludicola serrana here considered to be a
junior synonym of Pseudopaludicola murundu Geographi-cal distribution of Pseudopaludicola murundu as presentlyrecognized is not anymore restricted to its type-locality [16]but includes instead twelve distinct localities in southeasternBrazil in the states of Minas Gerais and Sao Paulo (Figure 7)
4 Discussion
41 Geographical Variation in Pseudopaludicola mystacalis(Cope 1887) Among the 18 valid species of Pseudopalu-dicola P mystacalis is currently the one with the mostwidespread distribution range Extent of occurrence in Brazilis nearly two million square kilometers encompassing areasin three different ecoregions along all the ldquodiagonal of openformationsrdquo from South America [23] Caatinga Cerradoand Pantanal It is also found in areas of Chaco in Argentina[24] and Paraguay [25] Although plausible the occurrence inBolivian Chaco was based on material that morphologicallyand bioacoustically would correspond to P ameghini [12 26]Habitats where individuals of this species were found includeldquorestingardquo [10 present study] ldquocampo sujordquo in elevatedplateaus of theCerradoDomain and seasonally floodedfieldsin the Pantanal lowlands [8]
Advertisement calls of Pseudopaludicola mystacalis fromdifferent Brazilian localities are composed of series of noteswith concatenated pulses Maximum variation in dominantfrequency of the calls of all specimens analyzed is 8613Hz(from 44789Hz in Cuiaba Mato Grosso to 53402Hz inBalsas Maranhao Table 3) without any evident latitudinalor longitudinal trend Dominant frequency in the mostdistant known locations (Primavera state of Para and Icemstate of Sao Paulo) varied by 3721 Hz Considering subsetsof populations from Brazilian Northeast (states of CearaMaranhao and Piauı) and from Brazilian Midwest (statesof Mato Grosso and Goias) maximum interpopulationalvariation in dominant frequency is 646Hz and 7752Hzrespectively Maximum intrapopulational variation in dom-inant frequency evaluated for four localities in the lowerportion of the speciesrsquo range (Caceres Cuiaba Nossa Senhorado Livramento and Pocone state ofMatoGrosso) is 5168Hzin Cuiaba (see Table 3 and [8])
8 Advances in Zoology
3
2
1
0
minus1
minus2
210minus1minus2minus3
DF2
(37
)
DF1 (63)
(a)
3
2
1
0
minus1
minus2
minus3
3210minus1minus2minus3minus4
DF2
(15
)
DF1 (85)
(b)
2
1
0
minus1
210minus1minus2
DF1 (79)
DF2
(21
)
Chapada dos Guimaraes-MTCuiab a-MTNS Livramento-MTPorto Estrela-MTC aceres-MTBarra do Garccedilas-MTPocon e-MTUruaccedilu-GO
Alto Alegre-SP
Primavera-PAItapipoca-CETaBalsas-MABrejo do Piauı-PIacute
ıba-CE
Ic em-SP
(c)
Figure 3 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of 101 males (a) 37 females (b)and six bioacoustic variables (c) of Pseudopaludicola mystacalis from 15 different localities in Brazil
Maximum variation in temporal variables (notes perminute and number of pulses) of the calls of all specimensanalyzed is 2136 notesmin and 8 pulsesnote In the mostdistant known locations the difference in the number of notesper minute and in the number of pulses is 1003 notesmin
and 6 pulsesnote respectively Considering subsets of pop-ulations from Brazilian Northeast and Brazilian Midwestmaximum interpopulational variation is 1146 notesmin and1335 notesmin respectively There are 7 pulsesnote in callsfrom populations of both areas Maximum intrapopulational
Advances in Zoology 9
Pseudopaludicola serrana Pseudopaludicola murundu Pseudopaludicola saltica
05 1 15 2 25 3 35 4 45 5
A B C D E F G H I(k
Hz)
8
7
6
5
4
3
2
1
(s)
Figure 4 Spectrograms (DFT size = 512 samples two notes for each locality) of advertisement calls of Pseudopaludicola serrana (AndashC) andP murundu (DndashF) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais-Uberlandia (G) state of MatoGrosso-Chapada dos Guimaraes (type-locality H) and Porto Estrela (I)
Note Pulses
(a) (b)
(c) (d)
(e) (f)
(g) (h)
Figure 5 Oscillograms of advertisement calls of Pseudopaludicola serrana (a)-(b) and P murundu (c)ndash(e) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais Uberlandia (f) state of Mato Grosso Chapada dos Guimaraes (type-locality (g))and Porto Estrela (h) Total time of each oscillogram corresponds to 05 s
10 Advances in Zoology
4
2
0
minus2
minus4
6420minus2minus4
DF2
(2
)
DF1 (98)
(a)
4
2
0
minus2
minus4
6420minus2minus4
DF2
(1
)
DF1 (99)
(b)
Figure 6 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of males (a) and six bioacousticvariables (b) of Pseudopaludicola murundu (open circles) P saltica (triangles) and P serrana (closed circles)
Elevation (m)
0
(km)
minus155ndash350351ndash700701ndash1050
1050ndash14001401ndash1750
300
N
1
2
3
4
5
6 78
91011
12
13
Figure 7 Geographical distribution of Pseudopaludicola murundu(circles) and P saltica (triangles) in southeastern Brazil state of SaoPaulomdashRioClaro (type locality (1)) andCampinas (2) state ofMinasGeraismdashPocos de Caldas (3) Alpinopolis (4) (see [17]) Sao Roquede Minas (5) Sao Joao Del Rei (6) Mariana (7) Ouro Branco (8)Itabirito (9) Brumadinho (10) Lavras Novas (11) Botumirim (12)and Uberlandia (13)
variation in the number of notes per minute and in thenumber of pulses in four localities from the state of MatoGrosso is 81 notesmin in Cuiaba and 5 pulsesnote in Cuiabaand Nossa Senhora do Livramento (see Table 3 and [8])Mean note duration does not differ significantly in all theexamined calls (Table 3 119865 = 49 df = 2 119875 = 003)
Table 5 Summary of the number of male specimens correctlyclassified as Pseudopaludicolamurundu P saltica or P serrana usingdiscriminant function analysis of 12 morphometric measurementsand seven bioacoustic variables
Morphometric measurementsTrue group
P murundu P saltica P serranaP murundu 1 0 5P saltica 0 39 0P serrana 3 0 19Total number 6 39 22 16 100 86
Bioacoustic variablesTrue group
P murundu P saltica P serranaP murundu 5 0 1P saltica 0 8 1P serrana 3 0 2Total number 6 9 5 83 889 40
Acoustic analysis of geographical variation in specieswith an extent of occurrence of the magnitude seen inP mystacalis sometimes reveals cryptic taxa being treatedunder a single name However this was not the case in Pmystacalis a taxon that remained erroneously characterizedand poorly recognized in the literature until recently [8] Ourresults reveal a relatively small variation in morphologicaland acoustical traits of P mystacalis and allow confirming thepresence of the species in a wide geographical area along theBrazilian open ecosystems
Advances in Zoology 11
Table 6 Ratios of selected measurements (in mm) of males of Pseudopaludicola murundu P salticaand P serrana Values are presented asmean plusmn standard deviation119873 = number of specimens analyzed
HLSVL HWSVL HLHW HALSVL FLSVL THLSVL TLSVLP serrana (119873 = 21) 040 plusmn 003 036 plusmn 002 110 plusmn 006 027 plusmn 002 061 plusmn 004 056 plusmn 003 070 plusmn 003
P murundu (119873 = 5) 039 plusmn 004 035 plusmn 003 111 plusmn 009 027 plusmn 001 066 plusmn 002 056 plusmn 002 070 plusmn 003
P saltica (119873 = 44) 041 plusmn 004 038 plusmn 003 109 plusmn 011 026 plusmn 003 068 plusmn 006 055 plusmn 005 073 plusmn 005
HAL hand length HL head length HW head width FL foot length SVL snout-vent length THL thigh length TL tibia length
42 Taxonomic Status of Pseudopaludicola serrana Toledo2010 When describing P serrana Toledo [15] used asmorphological characteristics separating the three speciesbelonging to the P saltica group the aspect (relative size andcoloration) of nuptial pads in the external part of finger I andaspect of the vocal sac Such characteristics allow differingP serrana and P murundu from P saltica but do not allowdiffering P serrana from P murundu [15] Previously Haddadand Cardoso [17] had called attention to the fact that nuptialpads were more developed in specimens of P saltica from thetype-locality (Chapada do Guimaraes Mato Grosso) than inspecimens collected and recorded in localities in the statesof Minas Gerais and Sao Paulo In the same article Haddadand Cardoso [17] also presented a spectrogram of the callof a specimen from Campinas Sao Paulo Based on suchreported morphological evidence and acoustic parameterswe here argue that specimens from Minas Gerais and SaoPaulo attributed to P saltica in Haddad and Cardoso [17] infact correspond to P murundu
The only external morphological characteristic used byToledo [15] to differ P serrana from P murunduwas a shorterhead lengthheadwidth ratio (HLHW= 097plusmn006 in the fiveindividuals ofP serrana evaluated 111plusmn007 in 11 individualsof P murundu) After having analyzed a higher number ofspecimens attributed to P serrana (119873 = 21) we found thatHLHW (110 plusmn 006 see Table 6) in this sample does notdiffer from the values presented in the original descriptionand confirmed herein for P murundu
The description of P serrana was also based on physicalcharacteristics of its advertisement calls [15] However theoriginal dataset is relatively low 12 notes of a single maleof P saltica 14 notes of 2 males of P murundu and 15notes of 3 males of P serrana were analyzed and comparedOnly one out of four acoustic variables (pulse duration) wasconsidered diagnostic for the new species Toledo [15] alsoshowed that dominant frequency range of P serrana wascompletely nested within the dominant frequency range of Pmurundu However when later proposing the synonymiza-tion of Pseudopaludicola riopiedadensis Mercadal de Bar-rio and Barrio 1994 to Pseudopaludicola ternetzi Miranda-Ribeiro 1937 Cardozo and Toledo [5] based their decision onldquoseveral important overlapsrdquo including dominant frequencyranges between the two species Indeed our data showedthat dominant frequency contributed to higher loadingsto separate species in the P saltica group Nonoverlappingdominant frequencies would therefore be expected betweenrelated but distinct species of Pseudopaludicola
Bioacoustic data have proven to be useful for uncoveringmorphologically cryptic species in the genus Pseudopaludi-cola [4ndash9 15 16] Advertisement calls of species in this genusmight be divided into three distinct groups according to typeof notes nonpulsed notes notes with concatenated pulsesand noteswith nonconcatenated pulses [7] Each groupmightbe diagnosed by temporal (pulses per note note and pulseduration internotes and interpulses intervals note rate andpulse rate) and spectral variables (dominant frequency andharmonics) which in combination allow characterizing allthe species for which calls were already analyzed except forP serrana and P murundu As evidenced by the recent syn-onymization of Pseudopaludicola riopiedadensis to P ternetzi[15] and reinforced herein by the proposed synonymizationof P serrana to P murundu morphologically similar speciesof Pseudopaludicola presenting the same type of note and anoverlap in their spectral acoustic variables are expected torepresent the same taxon Therefore no arguments remainto consider P serrana as a distinct species from P murunduand the former must be considered as a junior synonym of Pmurundu
5 Conclusions
We here report on the variation in morphometric charactersand variation in bioacoustic variables of the advertisementcalls in fifteen Brazilian populations of Pseudopaludicolamys-tacalis Although limited our sample evidenced no statisticaldifferences in any of the evaluated attributes and allowed usto confirm that this species is widely distributed in BrazilMorphometric and bioacoustic data did not differ also inpopulations currently attributed to Pseudopaludicola serranaand Pseudopaludicola murundu and the former taxon ishere considered as a junior synonym of P murundu Thedata in the present work aims at contributing to a betterunderstanding of the diversity and distribution patterns inthe genus Pseudopaludicola
Appendices
A Voucher Specimens Examined
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality 22∘1910158405210158401015840S 47∘4210158405610158401015840W)-F UFMT 18454MUFMT 18395-6 UFMT 18455-7
Pseudopaludicola mystacalis Brazil Para Primavera(00∘5710158402210158401015840S 47∘0710158401210158401015840W)-M UFMT 11651 UFMT 11827
12 Advances in Zoology
UFMT 11833 UFMT 11836 UFMT 11839 Goias Uruacu(14∘3110158403510158401015840S 49∘0710158405410158401015840W)-F UFMT 18397-400 UFMT18458-9 M UFMT 18401-15 UFMT 18458-64 Mato GrossoBarra do Garcas (15∘3110158405710158401015840S 52∘1410158401010158401015840W)-M UFMT11097 UFMT 11307 UFMT 11319 UFMT 11324 Caceres(16∘1710158405910158401015840S 58∘0910158400910158401015840W)-F UFMT 5906 UFMT 5950UFMT 5955 UFMT 5962 UFMT 9152 UFMT 10445UFMT 10448 UFMT 13669 M UFMT 10451-2 UFMT10455 UFMT 10458 UFMT 10466 UFMT 10495 UFMT10506 UFMT 10508 UFMT 13670 Chapada dos Guimaraes(type-locality 14∘5010158403410158401015840S 55∘2310158401010158401015840W)-F UFMT 8109 MUFMT 487 UFMT 817 UFMT 820 UFMT 12890 Cuiaba(15∘3910158403310158401015840S 55∘5610158403010158401015840W)-M UFMT 15980 UFMT 2426UFMT 2430 UFMT 2432 UFMT 2434-7 UFMT 2439UFMT 7399 UFMT 7653 UFMT 8177-8 UFMT 8180UFMT 8182 UFMT 8184-5 UFMT 13671 Nossa Senhorado Livramento (16∘2110158405810158401015840S 56∘1810158403310158401015840W)-F UFMT 18465UFMT 352 UFMT 6436 UFMT 6466-7 UFMT 6488UFMT 6511 M UFMT 4343 UFMT 6487 UFMT 6491UFMT6498UFMT6515Pocone (16∘3010158405810158401015840S 56∘4410158405310158401015840W)-M UFMT 348-50 UFMT 889 UFMT 4316 UFMT 4318UFMT 4321 UFMT 13672 and Porto Estrela (15∘3510158400510158401015840S57∘1310158402010158401015840W)-F UFMT 18466-7 UFMT 138 UFMT 13482M UFMT 18468-9 UFMT 402 UFMT 2200 UFMT 11346Sao Paulo Icem (20∘2010158403110158401015840S 49∘1110158404210158401015840W)-F UFMT 18421UFMT 18470-2 M UFMT 18422-3 UFMT 18473 and AltoAlegre (21∘3310158402010158401015840S 50∘1310158402210158401015840W)-F UFMT 18474-5 UFMT18479 MUFMT 18476-8 UFMT 18480-6
Pseudopaludicola saltica Brazil Mato Grosso Chapadados Guimaraes (type-locality 15∘2310158400910158401015840S 55∘5010158402410158401015840W)-MUFMT 482 UFMT 819 UFMT 821 UFMT 823 UFMT 1433-5 UFMT 1437-41 UFMT 2873 UFMT 2877 UFMT 2880-1F UFMT 1442 Cuiaba M UFMT 270 UFMT 473 UFMT476 UFMT 13657-68 F UFMT 13655-6) Nova Lacerda (MUFMT 13499-501) Porto Estrela Estacao Ecologica da Serradas Araras (M UFMT 561) and Vila Bela da SantıssimaTrindade (M UFMT 4082 UFMT 4112 UFMT 4123 UFMT4147 UFMT4153 UFMT4157 UFMT4172)MatoGrosso doSul Sonora (M UFMT 1147 UFMT 1195)
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho (type-locality 20∘0610158403210158401015840S 43∘5810158405310158401015840W)-F MCNAM 3675 MUFMT 18424 UFMT 18451 MCNAM 3677-8 MCNAM3680 Itabirito (20∘1310158402910158401015840S 43∘4810158404910158401015840W)-F MCNAM14620-1 M MCNAM 14625 Lavras Novas (20∘2810158405710158401015840S43∘3010158405210158401015840W)-F MCNAM 3694 M MCNAM 3695MCNAM 3690 Mariana (20∘0910158401210158401015840S 43∘3010158400210158401015840W)-FMCNAM 6465 M MCNAM 6457 MCNAM 6461-2 OuroBranco (20∘3010158401610158401015840S 43∘4210158400410158401015840W)-M MCNAM 6559 SaoJoao Del Rei (21∘0810158402510158401015840S 44∘1710158403110158401015840W)-M UFMT 18425-6UFMT 18452-3 and Botumirim (16∘4410158401310158401015840S 42∘3410158402910158401015840W)-FMCNAM 6713 M MCNAM 6832 MCNAM 6834 MCNAM6636 MCNAM 6642-3
B Analyzed Sound Files
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality) LH 676 no voucher specimen LH 677 call
fromUFMT 18455 LH 678 call fromUFMT 18395 and FNJV12976 no voucher specimen Minas Gerais Sao Roque deMinas (20∘1310158402010158401015840S 46∘2710158402410158401015840W) FNJV 4575 no voucherspecimen and Pocos de Caldas (21∘5510158400410158401015840S 46∘3410158400210158401015840W)FNJV 4576 no voucher specimen
Pseudopaludicola mystacalis Brazil Ceara Itapipoca(03∘2410158405810158401015840S 39∘4110158403110158401015840W) LH 655 no voucher specimenTaiba (03∘2510158404410158401015840S 38∘5710158404310158401015840W) LH 658 no voucher spec-imen Goias Uruacu LH 639 call from UFMT 18410) MatoGrosso Chapada dos Guimaraes (type-locality) LH 13A-05no voucher specimen) Caceres LH 47A-04 call fromUFMT10451 Cuiaba LH 14A-01 call from UFMT 2426 LH 14A-02 call from UFMT 2424 Pocone LH 01A-01 call fromUFMT 4321 and Nossa Senhora do Livramento LH 04A-10 call from UFMT 4330 Maranhao Balsa (07∘2810158404910158401015840S46∘0310158401910158401015840W) LH 284 no voucher specimen Piauı Brejo doPiauı (08∘1110158405010158401015840S 42∘4910158405910158401015840W) LH 184 call from UFMT11202 Para Primavera LH 352 call from UFMT 11836 SaoPaulo Icem LH 701 call from UFMT 18423
Pseudopaludicola saltica BrazilMatoGrossoCuiaba LH13A-01 call fromUFMT 8187Nova Lacerda LH 42A-06 callfrom UFMT 13499 LH 42A-07 call from UFMT 13500 andPorto Estrela LH 12 no voucher specimen LH 13 call fromUFMT 13678 LH 14 call fromUFMT 16423 LH 16 call fromUFMT 16417 LH 17 call from UFMT 16414 and LH 18 callfrom UFMT 16385 Minas Gerais Uberlandia (18∘5810158403010158401015840S48∘1710158402610158401015840W) LH 709 no voucher specimen
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho LH 673call from UFMT 18451 LH 674 no voucher specimen andSao Joao Del Rei LH 675 call from UFMT 18426 and FNJV12879-80 no voucher specimen
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Special thanks go to Felipe Franco Curcio Diva MariaBorges-Nojosa and Luciana Barreto Nascimento for allow-ing access to the material under their care at ldquoColecaoZoologica de Vertebrados da Universidade Federal de MatoGrossordquo (UFMT) ldquoColecao Herpetologica da UniversidadeFederal do Cearardquo (UFC) and ldquoMuseu de Ciencias Naturaisrdquo(MCNAM Belo Horizonte Minas Gerais) respectively toAdao J Cardoso (in memoriam) and Luis F Toledo for therecordings and for allowing access respectively to bioa-coustic samples deposited at ldquoFonoteca Neotropical JacquesVielliardrdquo (FNJV) to the CNPq project ldquoRede de pesquisa emanfıbios e repteis de ecossistemas nao florestais brasileirosrdquo(Process no 5633522010-8) for logistical support to VivianUhlig (RANICMBio) for estimates of extent of occurrenceAndre Pansonato thanks ldquoCoordenacao de Aperfeicoamentode Pessoal de Nivel Superiorrdquo (CAPES) for a PhD scholar-ship and Christine Strussmann thanks CNPq for a researchfellowship (Process no 3095412012-3)
Advances in Zoology 13
References
[1] K D Wells The Ecology amp Behavior of Amphibians TheUniversity of Chicago Chicago Ill USA 2007
[2] M Vences M Gehara J Kohler and F Glaw ldquoDescription of anewMalagasy treefrog (Boophis) occurring syntopically with itssister species and a plea for studies on non-allopatric speciationin tropical amphibiansrdquo Amphibia Reptilia vol 33 no 3-4 pp503ndash520 2012
[3] I De La Riva R Marquez and J Bosch ldquoDescription ofthe advertisement calls of some South American Hylidae(Amphibia Anura) taxonomic and methodological conse-quencesrdquo Bonner Zoologische Beitrage vol 47 pp 175ndash185 1997
[4] F S de Andrade and T R de Carvalho ldquoA new species of Pseu-dopaludicola Miranda-Ribeiro (Leiuperinae LeptodactylidaeAnura) from the Cerrado of southeastern Brazilrdquo Zootaxa vol3608 no 5 pp 389ndash397 2013
[5] D Cardozo and L F Toledo ldquoTaxonomic status of Pseudopalu-dicola riopiedadensis Mercadal de Barrio and Barrio 1994(Anura Leptodactylidae Leiuperinae)rdquo Zootaxa vol 3734 pp571ndash582 2013
[6] T R de Carvalho ldquoA new species of PseudopaludicolaMiranda-Ribeiro (Leiuperinae Leptodactylidae Anura) from the Cer-rado of southeastern Brazil with a distinctive advertisement callpatternrdquo Zootaxa no 3328 pp 47ndash54 2012
[7] F M Magalhaes D Loebmann M N C Kokubum C F BHaddad and A A Garda ldquoA new species of Pseudopaludi-cola (Anura Leptodactylidae Leiuperinae) from NortheasternBrazilrdquo Herpetologica vol 70 pp 77ndash88 2014
[8] A Pansonato C Strussmann J R Mudrek and I A Mar-tins ldquoMorphometric and bioacoustic data on three species ofPseudopaludicola Miranda-Ribeiro 1926 (Anura Leptodactyl-idae Leiuperinae) described from Chapada dos GuimaraesMato Grosso Brazil with the revalidation of Pseudopaludicolaameghini (Cope 1887)rdquo Zootaxa vol 3620 no 1 pp 147ndash1622013
[9] I J Roberto D Cardozo and R W Avila ldquoA new speciesof Pseudopaludicola (Anura Leiuperidae) from Western PiauıState Northeast Brazilrdquo Zootaxa vol 3636 no 2 pp 348ndash3602013
[10] S B Barreto M S Tinoco D Couto-Ferreira and H CBrowne-Ribeiro ldquoDistribuicao de Pseudopaludicola aff falcipes(Anura Leiuperidae) na restinga do litoral norte da BahiaBrasilrdquoRevista Latino-Americana de Conservacao vol 2 pp 27ndash36 2012
[11] E R Favero A C P Veiga-Menoncello D C Rossa-Feres et alldquoIntrageneric karyotypic variation in Pseudopaludicola (AnuraLeiuperidae) and its taxonomic relatednessrdquo Zoological Studiesvol 50 no 6 pp 826ndash836 2011
[12] M Jansen R Bloch A Schulze andM Pfenninger ldquoIntegrativeinventory of Boliviarsquos lowland anurans reveals hidden diversityrdquoZoologica Scripta vol 40 no 6 pp 567ndash583 2011
[13] C P D Prado M Uetanabaro and C F B Haddad ldquoBreed-ing activity patterns reproductive modes and habitat use byanurans (Amphibia) in a seasonal environment in the PantanalBrazilrdquo Amphibia Reptilia vol 26 no 2 pp 211ndash221 2005
[14] R A Silva I A Martins and D C Rossa-Feres ldquoBioacustica esıtio de vocalizacao em taxocenoses de anfıbios de area abertano Noroeste Paulistardquo Biota Neotropica vol 8 pp 123ndash1342008
[15] L F Toledo ldquoDescription of a new species of PseudopaludicolaMiranda-Ribeiro 1926 from the state of Sao Paulo SoutheasternBrazil (Anura Leiuperidae)rdquoZootaxa no 2681 pp 47ndash56 2010
[16] L F Toledo S Siqueira T CDuarte A C P Veiga-MenoncelloS M Recco-Pimentel and C F B Haddad ldquoDescription of anew species of Pseudopaludicola Miranda-Ribeiro 1926 fromthe state of Sao Paulo Southeastern Brazil (Anura Leiuperi-dae)rdquo Zootaxa no 2496 pp 38ndash48 2010
[17] C F B Haddad and A J Cardoso ldquoTaxonomia de tres especiesde Pseudopaludicola (Anura Leptodactylidae)rdquo Papeis Avulsosde Zoologia vol 36 pp 287ndash300 1987
[18] T C Duarte A C P Veiga-Menoncello J F R Lima et alldquoChromosome analysis in Pseudopaludicola (Anura Leiuperi-dae) with description of sex chromosomes XXXY in P salticardquoHereditas vol 147 no 2 pp 43ndash52 2010
[19] A C P Veiga-Menoncello L B Lourenco C Strussmannet al ldquoA phylogenetic analysis of Pseudopaludicola (Anura)providing evidence of progressive chromosome reductionrdquoZoologica Scripta vol 43 no 3 pp 261ndash272 2014
[20] W R Heyer A S Rand C A G Cruz O L Peixoto and CE Nelson ldquoFrogs of Boraceiardquo Arquivos de Zoologia vol 31 pp231ndash410 1990
[21] W E Duellman The Hylid Frogs of Middle America vol 1 ofMonograph of the Museum of Natural History of University ofKansas 1970
[22] R Development Core Team The R Project for Statistical Com-puting Vienna Austria 2013 httpwwwr-projectorg
[23] P E Vanzolini ldquoEcological and geographical distribution oflizards in Pernambuco Northeastern Brasil (Sauria)rdquo PapeisAvulsos de Zoologia vol 18 no 4 pp 61ndash90 1974
[24] J M Cei ldquoAmphibians of Argentinardquo Monitore ZoologicoItaliano Nuova Serie Monografia vol 2 pp 1ndash609 1980
[25] F Brusquetti and E O Lavilla ldquoLista comentada de los anfibiosde ParaguayrdquoCuadernos deHerpetologıa vol 20 no 2 pp 3ndash792006
[26] I De La Riva J Kohler S Lotters and S Reichle ldquoTenyears of research on Bolivian amphibians updated checklistdistribution taxonomic problems literature and iconographyrdquoRevista Espanola Herpetologica vol 14 pp 19ndash164 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
2 Advances in Zoology
Table 1 Measurements (mm) of specimens of Pseudopaludicola mystacalis from localities in four Brazilian states Values are presented asmean plusmn standard deviation (minimumndashmaximum)119873 = number of specimens analyzed
Mato Grosso Sao Paulo Goias ParaMales Females Males Females Males Females Males
(119873 = 53) (119873 = 20) (119873 = 14) (119873 = 7) (119873 = 20) (119873 = 6) (119873 = 14)
SVL 139 plusmn 13 163 plusmn 09 139 plusmn 05 153 plusmn 07 141 plusmn 01 159 plusmn 09 154 plusmn 08
(109ndash163) (143ndash181) (13ndash149) (143ndash16) (117ndash165) (146ndash17) (146ndash166)
HL 54 plusmn 04 62 plusmn 05 54 plusmn 03 55 plusmn 03 53 plusmn 04 58 plusmn 05 56 plusmn 02
(44ndash65) (52ndash75) (46ndash59) (51ndash60) (47ndash61) (50ndash63) (53ndash59)
HW 48 plusmn 05 59 plusmn 06 48 plusmn 02 51 plusmn 04 49 plusmn 05 55 plusmn 04 48 plusmn 03
(37ndash67) (50ndash68) (43ndash51) (46ndash58) (43ndash64) (49ndash59) (45ndash53)
IOD 11 plusmn 02 14 plusmn 02 12 plusmn 01 13 plusmn 01 12 plusmn 02 14 plusmn 02 14 plusmn 02
(07ndash16) (08ndash17) (10ndash14) (11ndash14) (10ndash17) (12ndash18) (11ndash15)
ED 16 plusmn 02 17 plusmn 02 14 plusmn 01 15 plusmn 02 15 plusmn 01 16 plusmn 01 17 plusmn 008
(10ndash19) (13ndash23) (11ndash17) (13ndash19) (12ndash17) (14ndash18) (16ndash18)
END 12 plusmn 02 14 plusmn 02 11 plusmn 007 13 plusmn 02 12 plusmn 01 13 plusmn 01 12 plusmn 01
(07ndash18) (11ndash21) (10ndash12) (11ndash18) (09ndash15) (11ndash14) (11ndash14)
IND 12 plusmn 02 15 plusmn 02 13 plusmn 01 14 plusmn 009 14 plusmn 01 15 plusmn 02 13 plusmn 009
(08ndash17) (10ndash19) (11ndash15) (13ndash15) (11ndash17) (12ndash17) (12ndash14)
HAL 37 plusmn 03 44 plusmn 07 39 plusmn 02 42 plusmn 04 38 plusmn 02 41 plusmn 03 39 plusmn 02
(31ndash44) (32ndash63) (35ndash43) (38ndash48) (34ndash44) (38ndash45) (36ndash41)
THL 63 plusmn 05 77 plusmn 09 62 plusmn 03 66 plusmn 06 65 plusmn 05 74 plusmn 02 68 plusmn 02
(51ndash73) (64ndash94) (56ndash69) (53ndash71) (56ndash73) (71ndash77) (66ndash72)
TL 69 plusmn 05 83 plusmn 09 7 plusmn 03 75 plusmn 03 71 plusmn 04 78 plusmn 02 74 plusmn 02
(59ndash82) (72ndash98) (67ndash76) (71ndash78) (64ndash80) (75ndash81) (72ndash76)
TAL 39 plusmn 04 45 plusmn 06 39 plusmn 02 43 plusmn 03 39 plusmn 03 43 plusmn 03 39 plusmn 03
(31ndash46) (31ndash52) (35ndash45) (39ndash46) (32ndash45) (40ndash48) (34ndash42)
FL 77 plusmn 05 92 plusmn 08 79 plusmn 03 84 plusmn 05 77 plusmn 04 85 plusmn 06 81 plusmn 05
(63ndash92) (79ndash106) (73ndash84) (76ndash89) (69ndash82) (78ndash92) (76ndash88)
South American ldquodiagonal of open formationsrdquo [8] Howeversome populations along the speciesrsquo range are not recognizedas belonging to this taxon being rather attributed to othertaxonomic entities such as Pseudopaludicola aff falcipesPseudopaludicola aff mystacalis and Pseudopaludicola sp[10ndash14] Therefore an integrative taxonomic revision isneeded to clarify the distribution range and variation in thisspecies [9]
In spite of great morphological similarity among most ofthe 18 species of Pseudopaludicola currently recognized threeof them are readily distinguished from the others by havinglonger hindlimbs [4ndash6 8 9] Pseudopaludicola saltica (Cope1887) Pseudopaludicola murundu Toledo Siqueira DuarteVeiga-Menoncello Recco-Pimentel and Haddad 2010 andPseudopaludicola serrana Toledo 2010 Advertisement callsof all three species are similarly composed of series of noteswith nonconcatenated pulses [8 15ndash17] and they all share 2119899 =22 chromosomes [16 18] comprising a monophyletic clade[19] However the results of a recent molecular phylogeneticanalysis suggested that P serrana is a junior synonym of Pmurundu [19]
Objectives of the present article are (1) to provide andto discuss the intraspecific variation in morphological andbioacoustic traits of P mystacalis along its distribution rangein Brazil (2) to reassess the taxonomic status of P serranabased on the reinterpretation of the literature data and on theexamination of new materials (specimens and calls) freshlyobtained at the type-locality andor its vicinities of P serranaand related species
2 Material and Methods
Examined specimens of P mystacalis P murundu P salticaand P serrana (Appendices A and B) are deposited in thefollowing collections ldquoColecao Zoologica de VertebradosUniversidade Federal de Mato Grossordquo (UFMT CuiabaMato Grosso Brazil) ldquoColecao Herpetologica da Universi-dade Federal do Cearardquo (UFC Fortaleza Ceara) ldquoFonotecaNeotropical Jacques Vielliardrdquo (FNJV Campinas Sao Paulo)and ldquoMuseu de Ciencias Naturaisrdquo (MCNAM Belo Hor-izonte Minas Gerais) Material deposited at UFMT was
Advances in Zoology 3
Table 2 Measurements (mm) of the topotypes of Pseudopaludicola serrana and P murundu Values are presented as mean plusmn standarddeviation (minimumndashmaximum) Additional localities (state of Minas Gerais municipalities of Itabirito Lavras Novas Mariana OuroBranco Sao Joao Del Rei and Botumirim)119873 = number of specimens analyzed
Pseudopaludicola serrana Pseudopaludicola murunduTopotypes Additional localities Topotypes
Males Females Males Females Males Females(119873 = 5) (119873 = 1) (119873 = 16) (119873 = 5) (119873 = 5) (119873 = 1)
SVL 163 plusmn 12 177 152 plusmn 09 171 plusmn 12 159 plusmn 08 173(146ndash175) (126ndash167) (159ndash185) (152ndash169)
HL 65 plusmn 05 68 60 plusmn 04 67 plusmn 03 61 plusmn 04 68(62ndash73) (48ndash69) (63ndash71) (56ndash67)
HW 60 plusmn 02 66 55 plusmn 04 63 plusmn 03 55 plusmn 02 59(57ndash63) (47ndash61) (59ndash67) (53ndash58)
IOD 14 plusmn 01 18 14 plusmn 01 16 plusmn 007 14 plusmn 008 15(13ndash16) (12ndash16) (15ndash17) (13ndash15)
ED 16 plusmn 007 17 15 plusmn 01 16 plusmn 009 16 plusmn 02 19(15ndash17) (13ndash17) (15ndash17) (14ndash18)
END 16 plusmn 009 16 15 plusmn 01 15 plusmn 008 15 plusmn 008 16(15ndash17) (13ndash17) (14ndash16) (14ndash16)
IND 15 plusmn 01 18 14 plusmn 01 16 plusmn 008 15 plusmn 009 16(13ndash17) (12ndash17) (15ndash17) (14ndash17)
HAL 44 plusmn 01 49 41 plusmn 04 45 plusmn 01 43 plusmn 02 49(43ndash46) (34ndash46) (43ndash47) (42ndash46)
THL 90 plusmn 03 102 85 plusmn 07 94 plusmn 05 89 plusmn 03 95(85ndash93) (68ndash94) (87ndash101) (86ndash93)
TL 109 plusmn 03 127 107 plusmn 07 118 plusmn 05 112 plusmn 03 123(106ndash113) (89ndash115) (109ndash122) (108ndash116)
TAL 53 plusmn 02 58 51 plusmn 04 57 plusmn 04 54 plusmn 007 63(51ndash57) (42ndash55) (50ndash61) (54ndash56)
FL 98 plusmn 03 111 93 plusmn 08 102 plusmn 05 106 plusmn 04 114(95ndash103) (74ndash104) (95ndash106) (99ndash109)
collected with permission of the ldquoInstituto Chico Mendes deConservacao da Biodiversidaderdquo (ICMBIO 27231-1)
Since the available diagnoses for P serrana and Pmurundu do not allow clearly distinguishing specimens fromthese two species newmaterial from additional localities wasputatively associated with each of them based solely on thepositioning of collecting andor recording sites populationsfrom easternmost localities in Minas Gerais were consideredto represent P serrana and populations from westernmostlocalities in Minas Gerais (and those from the state of SaoPaulo) were considered to represent P murundu
The measurements of 218 adult specimens (Tables 1 and2) of P murundu (6 males 1 female) P mystacalis (101 males37 females) P saltica (39 males 3 females original data inPansonato et al [8]) and P serrana (22 males 6 females)were taken with a digital caliper to the nearest 01mmMeasurements for hand length (HAL) tibia length (TL)tarsus length (TAL) and foot length (FL) followedHeyer et al[20] Measurements for snout-vent length (SVL) head length(HL) head width (HW) interorbital distance (IOD) eye
diameter (ED) eye-nostril distance (END) internarial dis-tance (IND) and thigh length (THL) followedDuellman [21]
Vocalizations of specimens of Pmurundu Pmystacalis Psaltica andP serranawere recorded byAndre Pansonatowitha professional digital recorder Marantz PMD 660 equippedwith a Yoga EM-9600 external directional microphoneDigital recordings were sampled at 441 kHz sampling rateand 16 bit resolution and saved in uncompressed wave filesSpectrograms were edited using Raven Pro 13 software withthe following configuration for P mystacalis brightness 75contrast 80 DFT size 512 samples 3 dB filter bandwidth112Hz time grid overlap 50 forPmurunduP saltica andPserrana brightness 70 contrast 80 DFT size 512 samples3 dB filter bandwidth 124Hz time grid overlap 50
We analyzed 1894 notes (Tables 3 and 4) 503 from Pmurundu 444 notes from P mystacalis 577 from P salticaand 370 from P serrana The following temporal variableswere measured from the waveform number of pulses pernote note and pulse duration (ms) internote and interpulseinterval (ms) Note that repetition rate was calculated in
4 Advances in Zoology
Table 3 Measurements of bioacoustic variables of the advertisement calls of specimens of Pseudopaludicola mystacalis from 12 localities inseven Brazilian states (CE Ceara GO Goias MA Maranhao MT Mato Grosso PA Para PI Piauı SP Sao Paulo) Values are presented asmean plusmn standard deviation (minimumndashmaximum)119873 number of notes analyzed
LocalitymdashState Air temp Noteduration (ms)
Internoteinterval (ms)
Pulses pernote
Pulseduration (ms)
Dominantfrequency (Hz)
Notesmin(mean)
PoconemdashMT (119873 = 30) 256∘C 40 plusmn 5
(30ndash50)80 plusmn 10
(60ndash100)16 plusmn 12
(14ndash18)2 plusmn 03
(1-2)46842 plusmn 1157
(4522ndash49096)5111
NS LivramentomdashMT (119873 = 25) 252∘C 40 plusmn 4
(40ndash50)70 plusmn 30
(50ndash200)17 plusmn 10
(14ndash19)2 plusmn 03
(1-2)48114 plusmn 563
(47373ndash49096)5064
C GuimaraesmdashMT (119873 = 110) 263∘C 40 plusmn 4
(30ndash50)60 plusmn 10
(40ndash100)16 plusmn 08
(14ndash17)2 plusmn 04
(1-2)49624 plusmn 1815
(46512ndash52541)5769
CuiabamdashMT (119873 = 25) 26∘C 50 plusmn 4
(30ndash50)90 plusmn 10
(60ndash100)14 plusmn 08
(12ndash16)2 plusmn 04
(1ndash3)47752 plusmn 828
(46512ndash49096)4433
CuiabamdashMT (119873 = 25) 26∘C 45 plusmn 4
(30ndash50)80 plusmn 30
(50ndash200)16 plusmn 10
(13ndash18)2 plusmn 03
(1-2)48372 plusmn 150
(44789ndash49957)5243
CaceresmdashMT (119873 = 25) 26∘C 50 plusmn 3
(40ndash50)60 plusmn 50
(50ndash70)16 plusmn 10
(14ndash18)2 plusmn 03
(1-2)4901 plusmn 512
(47373ndash49957)5389
BalsasmdashMA (119873 = 30) 265∘C 40 plusmn 2
(37ndash45)80 plusmn 5
(70ndash90)16 plusmn 10
(14ndash18)2 plusmn 04
(1-2)507609 plusmn 20568
(47804ndash53402)5137
IcemmdashSP (119873 = 28) 23∘C 50 plusmn 5
(50ndash60)110 plusmn 7
(100ndash150)17 plusmn 17
(14ndash20)2 plusmn 04
(1-2)48722 plusmn 799
(47373ndash49742)3633
ItapipocamdashCE (119873 = 30) mdash 50 plusmn 3
(40ndash50)90 plusmn 10
(70ndash130)16 plusmn 12
(14ndash18)2 plusmn 04
(1-2)51282 plusmn 981
(47804ndash5211)4207
TaıbamdashCE (119873 = 30) mdash 40 plusmn 2
(40ndash50)70 plusmn 2
(60ndash70)16plusmn11(13ndash18)
2plusmn05(1ndash3)
47952plusmn852(46942ndash49526)
5353
Brejo do BuritimdashPI (119873 = 30) 27∘C 50 plusmn 1
(45ndash50)90 plusmn 20
(60ndash140)19 plusmn 06
(18ndash20) 2 486075 plusmn 3148
(48234ndash49096)4296
PrimaveramdashPA (119873 = 30) 255∘C 50 plusmn 2
(40ndash50)80 plusmn 5
(70ndash100)18plusmn12(16ndash20)
2plusmn05(1-2)
50406plusmn456(49219ndash51094)
4637
UruacumdashGO (119873 = 26) 245∘C 50plusmn2(40ndash50)
60plusmn5(50ndash80)
16plusmn12(14ndash18)
2 plusmn 05
(1-2)46334 plusmn 866
(4500ndash49688)5435
Mean plusmn SD 50 plusmn 4(30ndash60)
80 plusmn 10(40ndash200)
16 plusmn 17(12ndash20)
2 plusmn 04(1ndash3)
48874 plusmn 1495(44789ndash53402)
4901plusmn611(3633ndash5769)
notes perminute Dominant frequency (note peak frequencyHz) was obtained from the spectrogram Terminology forbioacoustic variables follows Magalhaes et al [7] Pansonatoet al [8] and Heyer et al [20] Vocalizations are archivedin the ldquoBanco de Registros Bioacusticosrdquo and housed at theldquoLaboratorio de Herpetologia do Instituto de Biociencias daUniversidade Federal de Mato Grossordquo (LH Cuiaba MatoGrosso)
Discriminant function analyses (DFA) were conducted inorder to evidence the set of morphometric and bioacousticvariables that mostly distinguish between the species ofPseudopaludicola compared herein DFA were performed oncorrelation matrices from 12 log-transformed morphometricand six bioacoustic variables using R platform version 301[22] Bioacoustic comparisons through the DFA were per-formed using mean individual values
3 Results
31 Geographical Variation in Pseudopaludicola mystacalis(Cope 1887) Based on morphology and bioacoustics Pseu-dopaludicola mystacalis was positively identified in fifteenlocalities (Figure 1) from seven Brazilian states Ceara Goias
Maranhao Mato Grosso Para Piauı and Sao Paulo Theadvertisement calls of Pseudopaludicola mystacalis along itsdistribution range in Brazil (Figures 1 and 2) consistedof series composed of 9ndash229 notes with 16 plusmn 17 (12ndash20)concatenated pulses (ie no interpulse intervals) Mean noterepetition rate was 4901 plusmn 611 notesmin (3633ndash5769)mean duration of each note was 50 plusmn 4ms (30ndash60) averageinternote interval varied from 80 plusmn 10ms (40ndash200) Meanpulse duration was 2 plusmn 04ms (1ndash3) Frequency ranged from26862Hz to 73433Hz and dominant frequency ranged from44789 to 53402Hz (Table 3)
Discriminant function analysis (DFA) with our dataon P mystacalis did not group localities neither regardingmorphometric characters (males and females) nor regardingbioacoustic variables The first function (DF1) of DFA withmorphometric data explained 63 of the variation amongmales of different populations (Figure 3(a)) and higherloadings corresponded to thigh length (105) hand length(98) and foot length (84) The DF1 explained 85 of thevariation among females (Figure 3(b)) and higher loadingscorresponded to hand length (123) foot length (107) andsnout-vent length (88) The DF1 of DFA with bioacousticvariables explained 79 of the total variation in our sample
Advances in Zoology 5
Table4
Measurementsof
bioacoustic
varia
bles
oftheadvertise
mentc
allsof
specim
enso
fPseud
opalud
icola
murun
duPsalticaandPserranaVa
lues
arepresentedas
meanplusmnsta
ndard
deviation(m
inim
umndashm
axim
um)
Species
(vou
cher
record)
Noted
uration(m
s)Internoteinterval(ms)
Pulse
duratio
n(m
s)Interpulsesinterval(ms)
Dom
inantfrequ
ency
(Hz)
Pulse
sno
teNotesm
inMun
icipality
state
Pmurun
du(LH676)
80plusmn12(58ndash105)
100plusmn15(69ndash
141)
8plusmn2(4ndash12)
26plusmn7(7ndash4
0)56007plusmn2043(5168ndash5857)33plusmn07(2ndash5)3489plusmn219(3145ndash3704)
RioClaroSP
Pmurun
du(LH677)
94plusmn11(49ndash
114)
98plusmn16(70ndash
140)
13plusmn2(9ndash17)
23plusmn9(6ndash39)
55799plusmn1502(52541ndash5857)29plusmn02(2-3)3172plusmn176(2956ndash3419)
RioClaroSP
Pmurun
du(LH678)
89plusmn13(33ndash104)
107plusmn12(89ndash
137)
9plusmn2(5ndash17)
20plusmn8(8ndash4
6)57259plusmn1297(53402ndash59001)37plusmn05(2ndash4
)3087plusmn139(2926ndash3264)
RioClaroSP
Pmurun
du(FNJV
12976)
81plusmn15(56ndash
103)
152plusmn50(79ndash
247)
9plusmn2(5ndash14)
18plusmn5(10ndash
29)
57557plusmn3226(5168ndash62016)37plusmn04(3-4)
2803
RioClaroSP
Pmurun
du(FNJV
4575)
81plusmn13(54ndash
105)
132plusmn20(97ndash193)
10plusmn2(5ndash16)
23plusmn9(5ndash50)
55755plusmn1493(4875ndash58125)34plusmn07(2ndash5)2843plusmn313(2182ndash3691)
SaoRo
qued
eMinasM
GPmurun
du(FNJV
4576)
118plusmn18(77ndash143)
159plusmn14(129ndash194)
13plusmn2(8ndash18)
27plusmn9(10ndash
54)
54603plusmn766(5250ndash
5625)36plusmn05(2ndash4
)2183plusmn198(1893ndash266
6)
Pocosd
eCaldasMG
Pserran
a(LH673)
98plusmn12(65ndash131)
184plusmn18(131ndash224)
12plusmn2(8ndash18)
16plusmn5(6ndash32)
56556plusmn1202(5168ndash5814)41plusmn03(3ndash5)2183plusmn74(2061ndash
2258)
Brum
adinho
MG
Pserran
a(LH674)
91plusmn14(49ndash
117)236plusmn25(184ndash288)
12plusmn2(6ndash17)
25plusmn8(5ndash4
1)53402plusmn293(5168ndash55125)29plusmn04(2ndash4
)1795plusmn84(1709ndash1877)
Brum
adinho
MG
Pserran
a(LH675)
83plusmn15(49ndash
99)
161plusmn51(81ndash197)
10plusmn2(7ndash16)
16plusmn7(5ndash33)
5857
37plusmn04(3-4)2494plusmn223(2282ndash2727)
SaoJoao
DelRe
iMG
Pserran
a(FNJV
12879)
60plusmn6(47ndash72)
86plusmn8(63ndash101)
8plusmn2(4ndash14)
8plusmn2(4ndash16)
57070plusmn1155(55125ndash5857)39plusmn03(3-4)4119plusmn237(3614ndash4
762)
SaoJoao
DelRe
iMG
Pserran
a(FNJV
12880)
63plusmn13(26ndash
97)
112plusmn20(75ndash166)
5plusmn1(1ndash
9)13plusmn5(4ndash33)
57737plusmn1693(55125ndash60293)38plusmn05(2ndash5)3487plusmn473(2511ndash
5172
)SaoJoao
DelRe
iMG
Psaltica
(13A
-01)
65plusmn9(48ndash86)
120plusmn19(75ndash170)
9plusmn2(5ndash13)
35plusmn14(5ndash55)
47510plusmn1042(460
81ndash49526)25plusmn05(2-3)3839plusmn36(3424ndash4
062)
Chapadad
osGuimaraesMT
Psaltica
(42A
-06)
58plusmn6(46ndash
70)
109plusmn14(90ndash
137)
8plusmn1(4ndash11)
15plusmn7(5ndash30)
49143plusmn353(48234ndash
49526)32plusmn03(3-4)3654plusmn419(2985ndash4
412)
Pontes
eLacerdaM
TPsaltica
(42A
-07)
66plusmn13(48ndash87)
186plusmn23(14
4ndash224)
11plusmn4(4ndash19)
36plusmn5(30ndash
46)
45004plusmn3398(40052ndash49526)22plusmn04(2-3)2393plusmn182(2135ndash283)
Pontes
eLacerdaM
TPsaltica
(LH12)
77plusmn8(63ndash95)
113plusmn18(80ndash
172)
6plusmn1(4ndash9
)21plusmn18(3ndash4
9)50230plusmn1357(48665ndash55125)39plusmn04(3ndash5)3183plusmn328(2299ndash3947)
PortoEstre
laM
TPsaltica
(LH13)
97plusmn6(85ndash106)
127plusmn10(99ndash
158)
5plusmn1(3ndash7)
18plusmn17(2ndash56)
52368plusmn615(50818
ndash52972
)5plusmn01(5ndash6
)2687plusmn147(2308ndash3141)
PortoEstre
laM
TPsaltica
(LH14)
78plusmn5(70ndash
92)
134plusmn17(107ndash210)
17plusmn13(4ndash4
4)6plusmn2(4ndash10)
48062plusmn677(46512
ndash49957)21plusmn03(2-3)2837plusmn253(2062ndash3389)
PortoEstre
laM
TPsaltica
(LH16)
97plusmn10(64ndash
118)
127plusmn18(93ndash162)
10plusmn3(6ndash18)
23plusmn17(3ndash56)
50359plusmn2998(43066ndash
5340
2)45plusmn06(3ndash5)2712plusmn265(2264ndash3352)
PortoEstre
laM
TPsaltica
(LH17)
73plusmn26(33ndash122)
106plusmn24(79ndash
228)
7plusmn1(4ndash8)
19plusmn13(5ndash54)
48837plusmn2099(44789ndash
5168)34plusmn05(3ndash5)3524plusmn776(2113ndash4
838)
PortoEstre
laM
TPsaltica
(LH18)
83plusmn4(75ndash100)
143plusmn17(100ndash212)
5plusmn2(3ndash16)
18plusmn14(3ndash4
7)52483plusmn443(50818
ndash52972
)41plusmn03(4-5)2670plusmn214(1987ndash
3389)
PortoEstre
laM
TPsaltica
(LH709)
86plusmn14(51ndash117
)122plusmn55(58ndash383)
6plusmn1(3ndash10)
11plusmn8(3ndash33)
51139plusmn1169(49967ndash5340
2)44plusmn05(4-5)3067plusmn725(1266ndash4
838)
Uberla
ndiaM
G
6 Advances in Zoology
60∘W 50
∘W 40∘W
0∘
10∘S
20∘S
30∘S
0 400
(km)
PA MA
PICE
4
5
6
MT
32
1
1
7
8
910
11
12
SP
GO
N
Figure 1 Geographical variation in the advertisement calls (oscillograms) of Pseudopaludicola mystacalis from twelve localities in sevenBrazilian states Para (PA) Primavera (1) Ceara (CE) Itapipoca (2) Taıba (3)Maranhao (MA) Balsas (4) Piauı (PI) Brejo do Piauı (5) Goias(GO) Uruacu (6) Mato Grosso (MT) Cuiaba (7) Chapada dos Guimaraes (8) Nossa Senhora do Livramento (9) Pocone (10) Caceres (11)Sao Paulo (SP) Icem (12) Total time of each oscillogram corresponds to 02 s
(Figure 3(c)) and higher loadings corresponded to note rate(385) internote interval (295) and note duration (221) Nodistinct groups were formed along the first function axis ofthe DFA
32 Taxonomic Status of Pseudopaludicola serrana Toledo2010 Advertisement calls of Pseudopaludicola serranarecorded at the type-locality (Brumadinho Minas Gerais)and nearly 120 km southwestwards at Serra do LenheiroMinas Gerais were similar to those of topotypes of P
murundu and distinct from topotypes of P saltica bothin spectral and temporal parameters (Figures 4 and 5)The intraspecific variation in bioacoustic parameters ofP murundu and P serrana presented below is based oncalls from topotypical specimens and on calls recorded inadditional localities listed in Appendix B
Advertisement calls of P serranawere composed of seriesof pulsed notes with nonconcatenated pulses Each note con-sisted of 36plusmn06 (range 2ndash5) pulses Mean note duration was82 plusmn 58ms (26ndash131) emitted on average at intervals of 167 plusmn58ms (63ndash288) Mean duration of each pulse was 9 plusmn 3ms
Advances in Zoology 7
Taiba(CE)
Uruaccedilu(GO)
BBuriti(PI)
C aceres
Livramento (MT)(MT)
(MT)(MT)
(MT) Pocon eCGuimaraes
Cuiab a Itapipoca(CE)
Primavera(PA)
Ic em(SP) Balsas
(MA)
(kH
z)8
7
6
5
4
3
2
1
(s)02 04 06 08 1 12 14 16 18 2 22 24 26 28 3 32 34 36 38
ı
Figure 2 Spectrograms (DFT size = 512 samples) of the advertisement calls of Pseudopaludicola mystacalis from twelve localities (two notesfor each locality) in seven Brazilian states (CE Ceara GO Goias MA Maranhao MT Mato Grosso PA Para PI Piauı SP Sao Paulo)
(2ndash18) Interpulse intervals were 16 plusmn 7ms long (4ndash41) Meanfrequency ranged from 40196 plusmn 453Hz to 70986 plusmn 312Hzand mean dominant frequency was 56251 plusmn 212Hz (5168ndash60293) Advertisement calls of Pmurunduwere composed ofseries of pulsed noteswith nonconcatenated pulses Each noteconsisted of 34 plusmn 06 (range 2ndash5) pulses Mean note durationwas 92 plusmn 18ms (33ndash143) emitted on average at intervals of121 plusmn 30ms (69ndash247) Mean duration of each pulse was 10 plusmn3ms (4ndash18) Interpulse intervals were 24plusmn8ms (5ndash54) Meanfrequency ranged from 36285 plusmn 513Hz to 73301 plusmn 355Hzand mean dominant frequency was 55901 plusmn 176Hz (4875ndash62016Hz)
A discriminant function analysis (DFA)withmorphome-tric data revealed that P serrana and P murundu overlappedalong the first function (DF1) ofDFAwhich explained 98ofthe total variation (Figure 6(a)) While the DFA did not sep-arate P serrana from P murundu both were separated froma third species (Pseudopaludicola saltica) whose individualsalso have long hindlimbs Higher loadings corresponded toeye diameter (121) tarsus length (75) and tibia length (46)DFA from bioacoustic data also separated Pseudopaludicolasaltica from P murundu and P serrana (Figure 6(b))The firstfunction (DF1) of DFA explained 99 of the total variationand higher loadings corresponded to dominant frequency(641) and number of pulses per note (61)
DFAofmorphometricmeasurements using all specimensassigned 100 of the individuals of Pseudopaludicola saltica86 of the individuals of P serrana and only 16 of theindividuals of P murundu to the correct species (Table 5)DFA of bioacoustic variables using all recorded males cor-rectly assigned 89 of the specimens of P saltica 83 of thespecimens of P murundu and 40 of P serrana (Table 5) Incontrast DFA with both morphometric and bioacoustic datausing specimens ofP saltica and amixed sample of specimensattributable to either P murundu or P serrana assigned 100of these latter to a single taxon
The overall similarity in morphology and general struc-ture of the call of P murundu and P serrana evidenced bythe results of DFA with 12 morphometric and six bioacous-tic variables strongly support the rejection of the specificstatus of Pseudopaludicola serrana here considered to be a
junior synonym of Pseudopaludicola murundu Geographi-cal distribution of Pseudopaludicola murundu as presentlyrecognized is not anymore restricted to its type-locality [16]but includes instead twelve distinct localities in southeasternBrazil in the states of Minas Gerais and Sao Paulo (Figure 7)
4 Discussion
41 Geographical Variation in Pseudopaludicola mystacalis(Cope 1887) Among the 18 valid species of Pseudopalu-dicola P mystacalis is currently the one with the mostwidespread distribution range Extent of occurrence in Brazilis nearly two million square kilometers encompassing areasin three different ecoregions along all the ldquodiagonal of openformationsrdquo from South America [23] Caatinga Cerradoand Pantanal It is also found in areas of Chaco in Argentina[24] and Paraguay [25] Although plausible the occurrence inBolivian Chaco was based on material that morphologicallyand bioacoustically would correspond to P ameghini [12 26]Habitats where individuals of this species were found includeldquorestingardquo [10 present study] ldquocampo sujordquo in elevatedplateaus of theCerradoDomain and seasonally floodedfieldsin the Pantanal lowlands [8]
Advertisement calls of Pseudopaludicola mystacalis fromdifferent Brazilian localities are composed of series of noteswith concatenated pulses Maximum variation in dominantfrequency of the calls of all specimens analyzed is 8613Hz(from 44789Hz in Cuiaba Mato Grosso to 53402Hz inBalsas Maranhao Table 3) without any evident latitudinalor longitudinal trend Dominant frequency in the mostdistant known locations (Primavera state of Para and Icemstate of Sao Paulo) varied by 3721 Hz Considering subsetsof populations from Brazilian Northeast (states of CearaMaranhao and Piauı) and from Brazilian Midwest (statesof Mato Grosso and Goias) maximum interpopulationalvariation in dominant frequency is 646Hz and 7752Hzrespectively Maximum intrapopulational variation in dom-inant frequency evaluated for four localities in the lowerportion of the speciesrsquo range (Caceres Cuiaba Nossa Senhorado Livramento and Pocone state ofMatoGrosso) is 5168Hzin Cuiaba (see Table 3 and [8])
8 Advances in Zoology
3
2
1
0
minus1
minus2
210minus1minus2minus3
DF2
(37
)
DF1 (63)
(a)
3
2
1
0
minus1
minus2
minus3
3210minus1minus2minus3minus4
DF2
(15
)
DF1 (85)
(b)
2
1
0
minus1
210minus1minus2
DF1 (79)
DF2
(21
)
Chapada dos Guimaraes-MTCuiab a-MTNS Livramento-MTPorto Estrela-MTC aceres-MTBarra do Garccedilas-MTPocon e-MTUruaccedilu-GO
Alto Alegre-SP
Primavera-PAItapipoca-CETaBalsas-MABrejo do Piauı-PIacute
ıba-CE
Ic em-SP
(c)
Figure 3 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of 101 males (a) 37 females (b)and six bioacoustic variables (c) of Pseudopaludicola mystacalis from 15 different localities in Brazil
Maximum variation in temporal variables (notes perminute and number of pulses) of the calls of all specimensanalyzed is 2136 notesmin and 8 pulsesnote In the mostdistant known locations the difference in the number of notesper minute and in the number of pulses is 1003 notesmin
and 6 pulsesnote respectively Considering subsets of pop-ulations from Brazilian Northeast and Brazilian Midwestmaximum interpopulational variation is 1146 notesmin and1335 notesmin respectively There are 7 pulsesnote in callsfrom populations of both areas Maximum intrapopulational
Advances in Zoology 9
Pseudopaludicola serrana Pseudopaludicola murundu Pseudopaludicola saltica
05 1 15 2 25 3 35 4 45 5
A B C D E F G H I(k
Hz)
8
7
6
5
4
3
2
1
(s)
Figure 4 Spectrograms (DFT size = 512 samples two notes for each locality) of advertisement calls of Pseudopaludicola serrana (AndashC) andP murundu (DndashF) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais-Uberlandia (G) state of MatoGrosso-Chapada dos Guimaraes (type-locality H) and Porto Estrela (I)
Note Pulses
(a) (b)
(c) (d)
(e) (f)
(g) (h)
Figure 5 Oscillograms of advertisement calls of Pseudopaludicola serrana (a)-(b) and P murundu (c)ndash(e) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais Uberlandia (f) state of Mato Grosso Chapada dos Guimaraes (type-locality (g))and Porto Estrela (h) Total time of each oscillogram corresponds to 05 s
10 Advances in Zoology
4
2
0
minus2
minus4
6420minus2minus4
DF2
(2
)
DF1 (98)
(a)
4
2
0
minus2
minus4
6420minus2minus4
DF2
(1
)
DF1 (99)
(b)
Figure 6 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of males (a) and six bioacousticvariables (b) of Pseudopaludicola murundu (open circles) P saltica (triangles) and P serrana (closed circles)
Elevation (m)
0
(km)
minus155ndash350351ndash700701ndash1050
1050ndash14001401ndash1750
300
N
1
2
3
4
5
6 78
91011
12
13
Figure 7 Geographical distribution of Pseudopaludicola murundu(circles) and P saltica (triangles) in southeastern Brazil state of SaoPaulomdashRioClaro (type locality (1)) andCampinas (2) state ofMinasGeraismdashPocos de Caldas (3) Alpinopolis (4) (see [17]) Sao Roquede Minas (5) Sao Joao Del Rei (6) Mariana (7) Ouro Branco (8)Itabirito (9) Brumadinho (10) Lavras Novas (11) Botumirim (12)and Uberlandia (13)
variation in the number of notes per minute and in thenumber of pulses in four localities from the state of MatoGrosso is 81 notesmin in Cuiaba and 5 pulsesnote in Cuiabaand Nossa Senhora do Livramento (see Table 3 and [8])Mean note duration does not differ significantly in all theexamined calls (Table 3 119865 = 49 df = 2 119875 = 003)
Table 5 Summary of the number of male specimens correctlyclassified as Pseudopaludicolamurundu P saltica or P serrana usingdiscriminant function analysis of 12 morphometric measurementsand seven bioacoustic variables
Morphometric measurementsTrue group
P murundu P saltica P serranaP murundu 1 0 5P saltica 0 39 0P serrana 3 0 19Total number 6 39 22 16 100 86
Bioacoustic variablesTrue group
P murundu P saltica P serranaP murundu 5 0 1P saltica 0 8 1P serrana 3 0 2Total number 6 9 5 83 889 40
Acoustic analysis of geographical variation in specieswith an extent of occurrence of the magnitude seen inP mystacalis sometimes reveals cryptic taxa being treatedunder a single name However this was not the case in Pmystacalis a taxon that remained erroneously characterizedand poorly recognized in the literature until recently [8] Ourresults reveal a relatively small variation in morphologicaland acoustical traits of P mystacalis and allow confirming thepresence of the species in a wide geographical area along theBrazilian open ecosystems
Advances in Zoology 11
Table 6 Ratios of selected measurements (in mm) of males of Pseudopaludicola murundu P salticaand P serrana Values are presented asmean plusmn standard deviation119873 = number of specimens analyzed
HLSVL HWSVL HLHW HALSVL FLSVL THLSVL TLSVLP serrana (119873 = 21) 040 plusmn 003 036 plusmn 002 110 plusmn 006 027 plusmn 002 061 plusmn 004 056 plusmn 003 070 plusmn 003
P murundu (119873 = 5) 039 plusmn 004 035 plusmn 003 111 plusmn 009 027 plusmn 001 066 plusmn 002 056 plusmn 002 070 plusmn 003
P saltica (119873 = 44) 041 plusmn 004 038 plusmn 003 109 plusmn 011 026 plusmn 003 068 plusmn 006 055 plusmn 005 073 plusmn 005
HAL hand length HL head length HW head width FL foot length SVL snout-vent length THL thigh length TL tibia length
42 Taxonomic Status of Pseudopaludicola serrana Toledo2010 When describing P serrana Toledo [15] used asmorphological characteristics separating the three speciesbelonging to the P saltica group the aspect (relative size andcoloration) of nuptial pads in the external part of finger I andaspect of the vocal sac Such characteristics allow differingP serrana and P murundu from P saltica but do not allowdiffering P serrana from P murundu [15] Previously Haddadand Cardoso [17] had called attention to the fact that nuptialpads were more developed in specimens of P saltica from thetype-locality (Chapada do Guimaraes Mato Grosso) than inspecimens collected and recorded in localities in the statesof Minas Gerais and Sao Paulo In the same article Haddadand Cardoso [17] also presented a spectrogram of the callof a specimen from Campinas Sao Paulo Based on suchreported morphological evidence and acoustic parameterswe here argue that specimens from Minas Gerais and SaoPaulo attributed to P saltica in Haddad and Cardoso [17] infact correspond to P murundu
The only external morphological characteristic used byToledo [15] to differ P serrana from P murunduwas a shorterhead lengthheadwidth ratio (HLHW= 097plusmn006 in the fiveindividuals ofP serrana evaluated 111plusmn007 in 11 individualsof P murundu) After having analyzed a higher number ofspecimens attributed to P serrana (119873 = 21) we found thatHLHW (110 plusmn 006 see Table 6) in this sample does notdiffer from the values presented in the original descriptionand confirmed herein for P murundu
The description of P serrana was also based on physicalcharacteristics of its advertisement calls [15] However theoriginal dataset is relatively low 12 notes of a single maleof P saltica 14 notes of 2 males of P murundu and 15notes of 3 males of P serrana were analyzed and comparedOnly one out of four acoustic variables (pulse duration) wasconsidered diagnostic for the new species Toledo [15] alsoshowed that dominant frequency range of P serrana wascompletely nested within the dominant frequency range of Pmurundu However when later proposing the synonymiza-tion of Pseudopaludicola riopiedadensis Mercadal de Bar-rio and Barrio 1994 to Pseudopaludicola ternetzi Miranda-Ribeiro 1937 Cardozo and Toledo [5] based their decision onldquoseveral important overlapsrdquo including dominant frequencyranges between the two species Indeed our data showedthat dominant frequency contributed to higher loadingsto separate species in the P saltica group Nonoverlappingdominant frequencies would therefore be expected betweenrelated but distinct species of Pseudopaludicola
Bioacoustic data have proven to be useful for uncoveringmorphologically cryptic species in the genus Pseudopaludi-cola [4ndash9 15 16] Advertisement calls of species in this genusmight be divided into three distinct groups according to typeof notes nonpulsed notes notes with concatenated pulsesand noteswith nonconcatenated pulses [7] Each groupmightbe diagnosed by temporal (pulses per note note and pulseduration internotes and interpulses intervals note rate andpulse rate) and spectral variables (dominant frequency andharmonics) which in combination allow characterizing allthe species for which calls were already analyzed except forP serrana and P murundu As evidenced by the recent syn-onymization of Pseudopaludicola riopiedadensis to P ternetzi[15] and reinforced herein by the proposed synonymizationof P serrana to P murundu morphologically similar speciesof Pseudopaludicola presenting the same type of note and anoverlap in their spectral acoustic variables are expected torepresent the same taxon Therefore no arguments remainto consider P serrana as a distinct species from P murunduand the former must be considered as a junior synonym of Pmurundu
5 Conclusions
We here report on the variation in morphometric charactersand variation in bioacoustic variables of the advertisementcalls in fifteen Brazilian populations of Pseudopaludicolamys-tacalis Although limited our sample evidenced no statisticaldifferences in any of the evaluated attributes and allowed usto confirm that this species is widely distributed in BrazilMorphometric and bioacoustic data did not differ also inpopulations currently attributed to Pseudopaludicola serranaand Pseudopaludicola murundu and the former taxon ishere considered as a junior synonym of P murundu Thedata in the present work aims at contributing to a betterunderstanding of the diversity and distribution patterns inthe genus Pseudopaludicola
Appendices
A Voucher Specimens Examined
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality 22∘1910158405210158401015840S 47∘4210158405610158401015840W)-F UFMT 18454MUFMT 18395-6 UFMT 18455-7
Pseudopaludicola mystacalis Brazil Para Primavera(00∘5710158402210158401015840S 47∘0710158401210158401015840W)-M UFMT 11651 UFMT 11827
12 Advances in Zoology
UFMT 11833 UFMT 11836 UFMT 11839 Goias Uruacu(14∘3110158403510158401015840S 49∘0710158405410158401015840W)-F UFMT 18397-400 UFMT18458-9 M UFMT 18401-15 UFMT 18458-64 Mato GrossoBarra do Garcas (15∘3110158405710158401015840S 52∘1410158401010158401015840W)-M UFMT11097 UFMT 11307 UFMT 11319 UFMT 11324 Caceres(16∘1710158405910158401015840S 58∘0910158400910158401015840W)-F UFMT 5906 UFMT 5950UFMT 5955 UFMT 5962 UFMT 9152 UFMT 10445UFMT 10448 UFMT 13669 M UFMT 10451-2 UFMT10455 UFMT 10458 UFMT 10466 UFMT 10495 UFMT10506 UFMT 10508 UFMT 13670 Chapada dos Guimaraes(type-locality 14∘5010158403410158401015840S 55∘2310158401010158401015840W)-F UFMT 8109 MUFMT 487 UFMT 817 UFMT 820 UFMT 12890 Cuiaba(15∘3910158403310158401015840S 55∘5610158403010158401015840W)-M UFMT 15980 UFMT 2426UFMT 2430 UFMT 2432 UFMT 2434-7 UFMT 2439UFMT 7399 UFMT 7653 UFMT 8177-8 UFMT 8180UFMT 8182 UFMT 8184-5 UFMT 13671 Nossa Senhorado Livramento (16∘2110158405810158401015840S 56∘1810158403310158401015840W)-F UFMT 18465UFMT 352 UFMT 6436 UFMT 6466-7 UFMT 6488UFMT 6511 M UFMT 4343 UFMT 6487 UFMT 6491UFMT6498UFMT6515Pocone (16∘3010158405810158401015840S 56∘4410158405310158401015840W)-M UFMT 348-50 UFMT 889 UFMT 4316 UFMT 4318UFMT 4321 UFMT 13672 and Porto Estrela (15∘3510158400510158401015840S57∘1310158402010158401015840W)-F UFMT 18466-7 UFMT 138 UFMT 13482M UFMT 18468-9 UFMT 402 UFMT 2200 UFMT 11346Sao Paulo Icem (20∘2010158403110158401015840S 49∘1110158404210158401015840W)-F UFMT 18421UFMT 18470-2 M UFMT 18422-3 UFMT 18473 and AltoAlegre (21∘3310158402010158401015840S 50∘1310158402210158401015840W)-F UFMT 18474-5 UFMT18479 MUFMT 18476-8 UFMT 18480-6
Pseudopaludicola saltica Brazil Mato Grosso Chapadados Guimaraes (type-locality 15∘2310158400910158401015840S 55∘5010158402410158401015840W)-MUFMT 482 UFMT 819 UFMT 821 UFMT 823 UFMT 1433-5 UFMT 1437-41 UFMT 2873 UFMT 2877 UFMT 2880-1F UFMT 1442 Cuiaba M UFMT 270 UFMT 473 UFMT476 UFMT 13657-68 F UFMT 13655-6) Nova Lacerda (MUFMT 13499-501) Porto Estrela Estacao Ecologica da Serradas Araras (M UFMT 561) and Vila Bela da SantıssimaTrindade (M UFMT 4082 UFMT 4112 UFMT 4123 UFMT4147 UFMT4153 UFMT4157 UFMT4172)MatoGrosso doSul Sonora (M UFMT 1147 UFMT 1195)
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho (type-locality 20∘0610158403210158401015840S 43∘5810158405310158401015840W)-F MCNAM 3675 MUFMT 18424 UFMT 18451 MCNAM 3677-8 MCNAM3680 Itabirito (20∘1310158402910158401015840S 43∘4810158404910158401015840W)-F MCNAM14620-1 M MCNAM 14625 Lavras Novas (20∘2810158405710158401015840S43∘3010158405210158401015840W)-F MCNAM 3694 M MCNAM 3695MCNAM 3690 Mariana (20∘0910158401210158401015840S 43∘3010158400210158401015840W)-FMCNAM 6465 M MCNAM 6457 MCNAM 6461-2 OuroBranco (20∘3010158401610158401015840S 43∘4210158400410158401015840W)-M MCNAM 6559 SaoJoao Del Rei (21∘0810158402510158401015840S 44∘1710158403110158401015840W)-M UFMT 18425-6UFMT 18452-3 and Botumirim (16∘4410158401310158401015840S 42∘3410158402910158401015840W)-FMCNAM 6713 M MCNAM 6832 MCNAM 6834 MCNAM6636 MCNAM 6642-3
B Analyzed Sound Files
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality) LH 676 no voucher specimen LH 677 call
fromUFMT 18455 LH 678 call fromUFMT 18395 and FNJV12976 no voucher specimen Minas Gerais Sao Roque deMinas (20∘1310158402010158401015840S 46∘2710158402410158401015840W) FNJV 4575 no voucherspecimen and Pocos de Caldas (21∘5510158400410158401015840S 46∘3410158400210158401015840W)FNJV 4576 no voucher specimen
Pseudopaludicola mystacalis Brazil Ceara Itapipoca(03∘2410158405810158401015840S 39∘4110158403110158401015840W) LH 655 no voucher specimenTaiba (03∘2510158404410158401015840S 38∘5710158404310158401015840W) LH 658 no voucher spec-imen Goias Uruacu LH 639 call from UFMT 18410) MatoGrosso Chapada dos Guimaraes (type-locality) LH 13A-05no voucher specimen) Caceres LH 47A-04 call fromUFMT10451 Cuiaba LH 14A-01 call from UFMT 2426 LH 14A-02 call from UFMT 2424 Pocone LH 01A-01 call fromUFMT 4321 and Nossa Senhora do Livramento LH 04A-10 call from UFMT 4330 Maranhao Balsa (07∘2810158404910158401015840S46∘0310158401910158401015840W) LH 284 no voucher specimen Piauı Brejo doPiauı (08∘1110158405010158401015840S 42∘4910158405910158401015840W) LH 184 call from UFMT11202 Para Primavera LH 352 call from UFMT 11836 SaoPaulo Icem LH 701 call from UFMT 18423
Pseudopaludicola saltica BrazilMatoGrossoCuiaba LH13A-01 call fromUFMT 8187Nova Lacerda LH 42A-06 callfrom UFMT 13499 LH 42A-07 call from UFMT 13500 andPorto Estrela LH 12 no voucher specimen LH 13 call fromUFMT 13678 LH 14 call fromUFMT 16423 LH 16 call fromUFMT 16417 LH 17 call from UFMT 16414 and LH 18 callfrom UFMT 16385 Minas Gerais Uberlandia (18∘5810158403010158401015840S48∘1710158402610158401015840W) LH 709 no voucher specimen
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho LH 673call from UFMT 18451 LH 674 no voucher specimen andSao Joao Del Rei LH 675 call from UFMT 18426 and FNJV12879-80 no voucher specimen
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Special thanks go to Felipe Franco Curcio Diva MariaBorges-Nojosa and Luciana Barreto Nascimento for allow-ing access to the material under their care at ldquoColecaoZoologica de Vertebrados da Universidade Federal de MatoGrossordquo (UFMT) ldquoColecao Herpetologica da UniversidadeFederal do Cearardquo (UFC) and ldquoMuseu de Ciencias Naturaisrdquo(MCNAM Belo Horizonte Minas Gerais) respectively toAdao J Cardoso (in memoriam) and Luis F Toledo for therecordings and for allowing access respectively to bioa-coustic samples deposited at ldquoFonoteca Neotropical JacquesVielliardrdquo (FNJV) to the CNPq project ldquoRede de pesquisa emanfıbios e repteis de ecossistemas nao florestais brasileirosrdquo(Process no 5633522010-8) for logistical support to VivianUhlig (RANICMBio) for estimates of extent of occurrenceAndre Pansonato thanks ldquoCoordenacao de Aperfeicoamentode Pessoal de Nivel Superiorrdquo (CAPES) for a PhD scholar-ship and Christine Strussmann thanks CNPq for a researchfellowship (Process no 3095412012-3)
Advances in Zoology 13
References
[1] K D Wells The Ecology amp Behavior of Amphibians TheUniversity of Chicago Chicago Ill USA 2007
[2] M Vences M Gehara J Kohler and F Glaw ldquoDescription of anewMalagasy treefrog (Boophis) occurring syntopically with itssister species and a plea for studies on non-allopatric speciationin tropical amphibiansrdquo Amphibia Reptilia vol 33 no 3-4 pp503ndash520 2012
[3] I De La Riva R Marquez and J Bosch ldquoDescription ofthe advertisement calls of some South American Hylidae(Amphibia Anura) taxonomic and methodological conse-quencesrdquo Bonner Zoologische Beitrage vol 47 pp 175ndash185 1997
[4] F S de Andrade and T R de Carvalho ldquoA new species of Pseu-dopaludicola Miranda-Ribeiro (Leiuperinae LeptodactylidaeAnura) from the Cerrado of southeastern Brazilrdquo Zootaxa vol3608 no 5 pp 389ndash397 2013
[5] D Cardozo and L F Toledo ldquoTaxonomic status of Pseudopalu-dicola riopiedadensis Mercadal de Barrio and Barrio 1994(Anura Leptodactylidae Leiuperinae)rdquo Zootaxa vol 3734 pp571ndash582 2013
[6] T R de Carvalho ldquoA new species of PseudopaludicolaMiranda-Ribeiro (Leiuperinae Leptodactylidae Anura) from the Cer-rado of southeastern Brazil with a distinctive advertisement callpatternrdquo Zootaxa no 3328 pp 47ndash54 2012
[7] F M Magalhaes D Loebmann M N C Kokubum C F BHaddad and A A Garda ldquoA new species of Pseudopaludi-cola (Anura Leptodactylidae Leiuperinae) from NortheasternBrazilrdquo Herpetologica vol 70 pp 77ndash88 2014
[8] A Pansonato C Strussmann J R Mudrek and I A Mar-tins ldquoMorphometric and bioacoustic data on three species ofPseudopaludicola Miranda-Ribeiro 1926 (Anura Leptodactyl-idae Leiuperinae) described from Chapada dos GuimaraesMato Grosso Brazil with the revalidation of Pseudopaludicolaameghini (Cope 1887)rdquo Zootaxa vol 3620 no 1 pp 147ndash1622013
[9] I J Roberto D Cardozo and R W Avila ldquoA new speciesof Pseudopaludicola (Anura Leiuperidae) from Western PiauıState Northeast Brazilrdquo Zootaxa vol 3636 no 2 pp 348ndash3602013
[10] S B Barreto M S Tinoco D Couto-Ferreira and H CBrowne-Ribeiro ldquoDistribuicao de Pseudopaludicola aff falcipes(Anura Leiuperidae) na restinga do litoral norte da BahiaBrasilrdquoRevista Latino-Americana de Conservacao vol 2 pp 27ndash36 2012
[11] E R Favero A C P Veiga-Menoncello D C Rossa-Feres et alldquoIntrageneric karyotypic variation in Pseudopaludicola (AnuraLeiuperidae) and its taxonomic relatednessrdquo Zoological Studiesvol 50 no 6 pp 826ndash836 2011
[12] M Jansen R Bloch A Schulze andM Pfenninger ldquoIntegrativeinventory of Boliviarsquos lowland anurans reveals hidden diversityrdquoZoologica Scripta vol 40 no 6 pp 567ndash583 2011
[13] C P D Prado M Uetanabaro and C F B Haddad ldquoBreed-ing activity patterns reproductive modes and habitat use byanurans (Amphibia) in a seasonal environment in the PantanalBrazilrdquo Amphibia Reptilia vol 26 no 2 pp 211ndash221 2005
[14] R A Silva I A Martins and D C Rossa-Feres ldquoBioacustica esıtio de vocalizacao em taxocenoses de anfıbios de area abertano Noroeste Paulistardquo Biota Neotropica vol 8 pp 123ndash1342008
[15] L F Toledo ldquoDescription of a new species of PseudopaludicolaMiranda-Ribeiro 1926 from the state of Sao Paulo SoutheasternBrazil (Anura Leiuperidae)rdquoZootaxa no 2681 pp 47ndash56 2010
[16] L F Toledo S Siqueira T CDuarte A C P Veiga-MenoncelloS M Recco-Pimentel and C F B Haddad ldquoDescription of anew species of Pseudopaludicola Miranda-Ribeiro 1926 fromthe state of Sao Paulo Southeastern Brazil (Anura Leiuperi-dae)rdquo Zootaxa no 2496 pp 38ndash48 2010
[17] C F B Haddad and A J Cardoso ldquoTaxonomia de tres especiesde Pseudopaludicola (Anura Leptodactylidae)rdquo Papeis Avulsosde Zoologia vol 36 pp 287ndash300 1987
[18] T C Duarte A C P Veiga-Menoncello J F R Lima et alldquoChromosome analysis in Pseudopaludicola (Anura Leiuperi-dae) with description of sex chromosomes XXXY in P salticardquoHereditas vol 147 no 2 pp 43ndash52 2010
[19] A C P Veiga-Menoncello L B Lourenco C Strussmannet al ldquoA phylogenetic analysis of Pseudopaludicola (Anura)providing evidence of progressive chromosome reductionrdquoZoologica Scripta vol 43 no 3 pp 261ndash272 2014
[20] W R Heyer A S Rand C A G Cruz O L Peixoto and CE Nelson ldquoFrogs of Boraceiardquo Arquivos de Zoologia vol 31 pp231ndash410 1990
[21] W E Duellman The Hylid Frogs of Middle America vol 1 ofMonograph of the Museum of Natural History of University ofKansas 1970
[22] R Development Core Team The R Project for Statistical Com-puting Vienna Austria 2013 httpwwwr-projectorg
[23] P E Vanzolini ldquoEcological and geographical distribution oflizards in Pernambuco Northeastern Brasil (Sauria)rdquo PapeisAvulsos de Zoologia vol 18 no 4 pp 61ndash90 1974
[24] J M Cei ldquoAmphibians of Argentinardquo Monitore ZoologicoItaliano Nuova Serie Monografia vol 2 pp 1ndash609 1980
[25] F Brusquetti and E O Lavilla ldquoLista comentada de los anfibiosde ParaguayrdquoCuadernos deHerpetologıa vol 20 no 2 pp 3ndash792006
[26] I De La Riva J Kohler S Lotters and S Reichle ldquoTenyears of research on Bolivian amphibians updated checklistdistribution taxonomic problems literature and iconographyrdquoRevista Espanola Herpetologica vol 14 pp 19ndash164 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
Advances in Zoology 3
Table 2 Measurements (mm) of the topotypes of Pseudopaludicola serrana and P murundu Values are presented as mean plusmn standarddeviation (minimumndashmaximum) Additional localities (state of Minas Gerais municipalities of Itabirito Lavras Novas Mariana OuroBranco Sao Joao Del Rei and Botumirim)119873 = number of specimens analyzed
Pseudopaludicola serrana Pseudopaludicola murunduTopotypes Additional localities Topotypes
Males Females Males Females Males Females(119873 = 5) (119873 = 1) (119873 = 16) (119873 = 5) (119873 = 5) (119873 = 1)
SVL 163 plusmn 12 177 152 plusmn 09 171 plusmn 12 159 plusmn 08 173(146ndash175) (126ndash167) (159ndash185) (152ndash169)
HL 65 plusmn 05 68 60 plusmn 04 67 plusmn 03 61 plusmn 04 68(62ndash73) (48ndash69) (63ndash71) (56ndash67)
HW 60 plusmn 02 66 55 plusmn 04 63 plusmn 03 55 plusmn 02 59(57ndash63) (47ndash61) (59ndash67) (53ndash58)
IOD 14 plusmn 01 18 14 plusmn 01 16 plusmn 007 14 plusmn 008 15(13ndash16) (12ndash16) (15ndash17) (13ndash15)
ED 16 plusmn 007 17 15 plusmn 01 16 plusmn 009 16 plusmn 02 19(15ndash17) (13ndash17) (15ndash17) (14ndash18)
END 16 plusmn 009 16 15 plusmn 01 15 plusmn 008 15 plusmn 008 16(15ndash17) (13ndash17) (14ndash16) (14ndash16)
IND 15 plusmn 01 18 14 plusmn 01 16 plusmn 008 15 plusmn 009 16(13ndash17) (12ndash17) (15ndash17) (14ndash17)
HAL 44 plusmn 01 49 41 plusmn 04 45 plusmn 01 43 plusmn 02 49(43ndash46) (34ndash46) (43ndash47) (42ndash46)
THL 90 plusmn 03 102 85 plusmn 07 94 plusmn 05 89 plusmn 03 95(85ndash93) (68ndash94) (87ndash101) (86ndash93)
TL 109 plusmn 03 127 107 plusmn 07 118 plusmn 05 112 plusmn 03 123(106ndash113) (89ndash115) (109ndash122) (108ndash116)
TAL 53 plusmn 02 58 51 plusmn 04 57 plusmn 04 54 plusmn 007 63(51ndash57) (42ndash55) (50ndash61) (54ndash56)
FL 98 plusmn 03 111 93 plusmn 08 102 plusmn 05 106 plusmn 04 114(95ndash103) (74ndash104) (95ndash106) (99ndash109)
collected with permission of the ldquoInstituto Chico Mendes deConservacao da Biodiversidaderdquo (ICMBIO 27231-1)
Since the available diagnoses for P serrana and Pmurundu do not allow clearly distinguishing specimens fromthese two species newmaterial from additional localities wasputatively associated with each of them based solely on thepositioning of collecting andor recording sites populationsfrom easternmost localities in Minas Gerais were consideredto represent P serrana and populations from westernmostlocalities in Minas Gerais (and those from the state of SaoPaulo) were considered to represent P murundu
The measurements of 218 adult specimens (Tables 1 and2) of P murundu (6 males 1 female) P mystacalis (101 males37 females) P saltica (39 males 3 females original data inPansonato et al [8]) and P serrana (22 males 6 females)were taken with a digital caliper to the nearest 01mmMeasurements for hand length (HAL) tibia length (TL)tarsus length (TAL) and foot length (FL) followedHeyer et al[20] Measurements for snout-vent length (SVL) head length(HL) head width (HW) interorbital distance (IOD) eye
diameter (ED) eye-nostril distance (END) internarial dis-tance (IND) and thigh length (THL) followedDuellman [21]
Vocalizations of specimens of Pmurundu Pmystacalis Psaltica andP serranawere recorded byAndre Pansonatowitha professional digital recorder Marantz PMD 660 equippedwith a Yoga EM-9600 external directional microphoneDigital recordings were sampled at 441 kHz sampling rateand 16 bit resolution and saved in uncompressed wave filesSpectrograms were edited using Raven Pro 13 software withthe following configuration for P mystacalis brightness 75contrast 80 DFT size 512 samples 3 dB filter bandwidth112Hz time grid overlap 50 forPmurunduP saltica andPserrana brightness 70 contrast 80 DFT size 512 samples3 dB filter bandwidth 124Hz time grid overlap 50
We analyzed 1894 notes (Tables 3 and 4) 503 from Pmurundu 444 notes from P mystacalis 577 from P salticaand 370 from P serrana The following temporal variableswere measured from the waveform number of pulses pernote note and pulse duration (ms) internote and interpulseinterval (ms) Note that repetition rate was calculated in
4 Advances in Zoology
Table 3 Measurements of bioacoustic variables of the advertisement calls of specimens of Pseudopaludicola mystacalis from 12 localities inseven Brazilian states (CE Ceara GO Goias MA Maranhao MT Mato Grosso PA Para PI Piauı SP Sao Paulo) Values are presented asmean plusmn standard deviation (minimumndashmaximum)119873 number of notes analyzed
LocalitymdashState Air temp Noteduration (ms)
Internoteinterval (ms)
Pulses pernote
Pulseduration (ms)
Dominantfrequency (Hz)
Notesmin(mean)
PoconemdashMT (119873 = 30) 256∘C 40 plusmn 5
(30ndash50)80 plusmn 10
(60ndash100)16 plusmn 12
(14ndash18)2 plusmn 03
(1-2)46842 plusmn 1157
(4522ndash49096)5111
NS LivramentomdashMT (119873 = 25) 252∘C 40 plusmn 4
(40ndash50)70 plusmn 30
(50ndash200)17 plusmn 10
(14ndash19)2 plusmn 03
(1-2)48114 plusmn 563
(47373ndash49096)5064
C GuimaraesmdashMT (119873 = 110) 263∘C 40 plusmn 4
(30ndash50)60 plusmn 10
(40ndash100)16 plusmn 08
(14ndash17)2 plusmn 04
(1-2)49624 plusmn 1815
(46512ndash52541)5769
CuiabamdashMT (119873 = 25) 26∘C 50 plusmn 4
(30ndash50)90 plusmn 10
(60ndash100)14 plusmn 08
(12ndash16)2 plusmn 04
(1ndash3)47752 plusmn 828
(46512ndash49096)4433
CuiabamdashMT (119873 = 25) 26∘C 45 plusmn 4
(30ndash50)80 plusmn 30
(50ndash200)16 plusmn 10
(13ndash18)2 plusmn 03
(1-2)48372 plusmn 150
(44789ndash49957)5243
CaceresmdashMT (119873 = 25) 26∘C 50 plusmn 3
(40ndash50)60 plusmn 50
(50ndash70)16 plusmn 10
(14ndash18)2 plusmn 03
(1-2)4901 plusmn 512
(47373ndash49957)5389
BalsasmdashMA (119873 = 30) 265∘C 40 plusmn 2
(37ndash45)80 plusmn 5
(70ndash90)16 plusmn 10
(14ndash18)2 plusmn 04
(1-2)507609 plusmn 20568
(47804ndash53402)5137
IcemmdashSP (119873 = 28) 23∘C 50 plusmn 5
(50ndash60)110 plusmn 7
(100ndash150)17 plusmn 17
(14ndash20)2 plusmn 04
(1-2)48722 plusmn 799
(47373ndash49742)3633
ItapipocamdashCE (119873 = 30) mdash 50 plusmn 3
(40ndash50)90 plusmn 10
(70ndash130)16 plusmn 12
(14ndash18)2 plusmn 04
(1-2)51282 plusmn 981
(47804ndash5211)4207
TaıbamdashCE (119873 = 30) mdash 40 plusmn 2
(40ndash50)70 plusmn 2
(60ndash70)16plusmn11(13ndash18)
2plusmn05(1ndash3)
47952plusmn852(46942ndash49526)
5353
Brejo do BuritimdashPI (119873 = 30) 27∘C 50 plusmn 1
(45ndash50)90 plusmn 20
(60ndash140)19 plusmn 06
(18ndash20) 2 486075 plusmn 3148
(48234ndash49096)4296
PrimaveramdashPA (119873 = 30) 255∘C 50 plusmn 2
(40ndash50)80 plusmn 5
(70ndash100)18plusmn12(16ndash20)
2plusmn05(1-2)
50406plusmn456(49219ndash51094)
4637
UruacumdashGO (119873 = 26) 245∘C 50plusmn2(40ndash50)
60plusmn5(50ndash80)
16plusmn12(14ndash18)
2 plusmn 05
(1-2)46334 plusmn 866
(4500ndash49688)5435
Mean plusmn SD 50 plusmn 4(30ndash60)
80 plusmn 10(40ndash200)
16 plusmn 17(12ndash20)
2 plusmn 04(1ndash3)
48874 plusmn 1495(44789ndash53402)
4901plusmn611(3633ndash5769)
notes perminute Dominant frequency (note peak frequencyHz) was obtained from the spectrogram Terminology forbioacoustic variables follows Magalhaes et al [7] Pansonatoet al [8] and Heyer et al [20] Vocalizations are archivedin the ldquoBanco de Registros Bioacusticosrdquo and housed at theldquoLaboratorio de Herpetologia do Instituto de Biociencias daUniversidade Federal de Mato Grossordquo (LH Cuiaba MatoGrosso)
Discriminant function analyses (DFA) were conducted inorder to evidence the set of morphometric and bioacousticvariables that mostly distinguish between the species ofPseudopaludicola compared herein DFA were performed oncorrelation matrices from 12 log-transformed morphometricand six bioacoustic variables using R platform version 301[22] Bioacoustic comparisons through the DFA were per-formed using mean individual values
3 Results
31 Geographical Variation in Pseudopaludicola mystacalis(Cope 1887) Based on morphology and bioacoustics Pseu-dopaludicola mystacalis was positively identified in fifteenlocalities (Figure 1) from seven Brazilian states Ceara Goias
Maranhao Mato Grosso Para Piauı and Sao Paulo Theadvertisement calls of Pseudopaludicola mystacalis along itsdistribution range in Brazil (Figures 1 and 2) consistedof series composed of 9ndash229 notes with 16 plusmn 17 (12ndash20)concatenated pulses (ie no interpulse intervals) Mean noterepetition rate was 4901 plusmn 611 notesmin (3633ndash5769)mean duration of each note was 50 plusmn 4ms (30ndash60) averageinternote interval varied from 80 plusmn 10ms (40ndash200) Meanpulse duration was 2 plusmn 04ms (1ndash3) Frequency ranged from26862Hz to 73433Hz and dominant frequency ranged from44789 to 53402Hz (Table 3)
Discriminant function analysis (DFA) with our dataon P mystacalis did not group localities neither regardingmorphometric characters (males and females) nor regardingbioacoustic variables The first function (DF1) of DFA withmorphometric data explained 63 of the variation amongmales of different populations (Figure 3(a)) and higherloadings corresponded to thigh length (105) hand length(98) and foot length (84) The DF1 explained 85 of thevariation among females (Figure 3(b)) and higher loadingscorresponded to hand length (123) foot length (107) andsnout-vent length (88) The DF1 of DFA with bioacousticvariables explained 79 of the total variation in our sample
Advances in Zoology 5
Table4
Measurementsof
bioacoustic
varia
bles
oftheadvertise
mentc
allsof
specim
enso
fPseud
opalud
icola
murun
duPsalticaandPserranaVa
lues
arepresentedas
meanplusmnsta
ndard
deviation(m
inim
umndashm
axim
um)
Species
(vou
cher
record)
Noted
uration(m
s)Internoteinterval(ms)
Pulse
duratio
n(m
s)Interpulsesinterval(ms)
Dom
inantfrequ
ency
(Hz)
Pulse
sno
teNotesm
inMun
icipality
state
Pmurun
du(LH676)
80plusmn12(58ndash105)
100plusmn15(69ndash
141)
8plusmn2(4ndash12)
26plusmn7(7ndash4
0)56007plusmn2043(5168ndash5857)33plusmn07(2ndash5)3489plusmn219(3145ndash3704)
RioClaroSP
Pmurun
du(LH677)
94plusmn11(49ndash
114)
98plusmn16(70ndash
140)
13plusmn2(9ndash17)
23plusmn9(6ndash39)
55799plusmn1502(52541ndash5857)29plusmn02(2-3)3172plusmn176(2956ndash3419)
RioClaroSP
Pmurun
du(LH678)
89plusmn13(33ndash104)
107plusmn12(89ndash
137)
9plusmn2(5ndash17)
20plusmn8(8ndash4
6)57259plusmn1297(53402ndash59001)37plusmn05(2ndash4
)3087plusmn139(2926ndash3264)
RioClaroSP
Pmurun
du(FNJV
12976)
81plusmn15(56ndash
103)
152plusmn50(79ndash
247)
9plusmn2(5ndash14)
18plusmn5(10ndash
29)
57557plusmn3226(5168ndash62016)37plusmn04(3-4)
2803
RioClaroSP
Pmurun
du(FNJV
4575)
81plusmn13(54ndash
105)
132plusmn20(97ndash193)
10plusmn2(5ndash16)
23plusmn9(5ndash50)
55755plusmn1493(4875ndash58125)34plusmn07(2ndash5)2843plusmn313(2182ndash3691)
SaoRo
qued
eMinasM
GPmurun
du(FNJV
4576)
118plusmn18(77ndash143)
159plusmn14(129ndash194)
13plusmn2(8ndash18)
27plusmn9(10ndash
54)
54603plusmn766(5250ndash
5625)36plusmn05(2ndash4
)2183plusmn198(1893ndash266
6)
Pocosd
eCaldasMG
Pserran
a(LH673)
98plusmn12(65ndash131)
184plusmn18(131ndash224)
12plusmn2(8ndash18)
16plusmn5(6ndash32)
56556plusmn1202(5168ndash5814)41plusmn03(3ndash5)2183plusmn74(2061ndash
2258)
Brum
adinho
MG
Pserran
a(LH674)
91plusmn14(49ndash
117)236plusmn25(184ndash288)
12plusmn2(6ndash17)
25plusmn8(5ndash4
1)53402plusmn293(5168ndash55125)29plusmn04(2ndash4
)1795plusmn84(1709ndash1877)
Brum
adinho
MG
Pserran
a(LH675)
83plusmn15(49ndash
99)
161plusmn51(81ndash197)
10plusmn2(7ndash16)
16plusmn7(5ndash33)
5857
37plusmn04(3-4)2494plusmn223(2282ndash2727)
SaoJoao
DelRe
iMG
Pserran
a(FNJV
12879)
60plusmn6(47ndash72)
86plusmn8(63ndash101)
8plusmn2(4ndash14)
8plusmn2(4ndash16)
57070plusmn1155(55125ndash5857)39plusmn03(3-4)4119plusmn237(3614ndash4
762)
SaoJoao
DelRe
iMG
Pserran
a(FNJV
12880)
63plusmn13(26ndash
97)
112plusmn20(75ndash166)
5plusmn1(1ndash
9)13plusmn5(4ndash33)
57737plusmn1693(55125ndash60293)38plusmn05(2ndash5)3487plusmn473(2511ndash
5172
)SaoJoao
DelRe
iMG
Psaltica
(13A
-01)
65plusmn9(48ndash86)
120plusmn19(75ndash170)
9plusmn2(5ndash13)
35plusmn14(5ndash55)
47510plusmn1042(460
81ndash49526)25plusmn05(2-3)3839plusmn36(3424ndash4
062)
Chapadad
osGuimaraesMT
Psaltica
(42A
-06)
58plusmn6(46ndash
70)
109plusmn14(90ndash
137)
8plusmn1(4ndash11)
15plusmn7(5ndash30)
49143plusmn353(48234ndash
49526)32plusmn03(3-4)3654plusmn419(2985ndash4
412)
Pontes
eLacerdaM
TPsaltica
(42A
-07)
66plusmn13(48ndash87)
186plusmn23(14
4ndash224)
11plusmn4(4ndash19)
36plusmn5(30ndash
46)
45004plusmn3398(40052ndash49526)22plusmn04(2-3)2393plusmn182(2135ndash283)
Pontes
eLacerdaM
TPsaltica
(LH12)
77plusmn8(63ndash95)
113plusmn18(80ndash
172)
6plusmn1(4ndash9
)21plusmn18(3ndash4
9)50230plusmn1357(48665ndash55125)39plusmn04(3ndash5)3183plusmn328(2299ndash3947)
PortoEstre
laM
TPsaltica
(LH13)
97plusmn6(85ndash106)
127plusmn10(99ndash
158)
5plusmn1(3ndash7)
18plusmn17(2ndash56)
52368plusmn615(50818
ndash52972
)5plusmn01(5ndash6
)2687plusmn147(2308ndash3141)
PortoEstre
laM
TPsaltica
(LH14)
78plusmn5(70ndash
92)
134plusmn17(107ndash210)
17plusmn13(4ndash4
4)6plusmn2(4ndash10)
48062plusmn677(46512
ndash49957)21plusmn03(2-3)2837plusmn253(2062ndash3389)
PortoEstre
laM
TPsaltica
(LH16)
97plusmn10(64ndash
118)
127plusmn18(93ndash162)
10plusmn3(6ndash18)
23plusmn17(3ndash56)
50359plusmn2998(43066ndash
5340
2)45plusmn06(3ndash5)2712plusmn265(2264ndash3352)
PortoEstre
laM
TPsaltica
(LH17)
73plusmn26(33ndash122)
106plusmn24(79ndash
228)
7plusmn1(4ndash8)
19plusmn13(5ndash54)
48837plusmn2099(44789ndash
5168)34plusmn05(3ndash5)3524plusmn776(2113ndash4
838)
PortoEstre
laM
TPsaltica
(LH18)
83plusmn4(75ndash100)
143plusmn17(100ndash212)
5plusmn2(3ndash16)
18plusmn14(3ndash4
7)52483plusmn443(50818
ndash52972
)41plusmn03(4-5)2670plusmn214(1987ndash
3389)
PortoEstre
laM
TPsaltica
(LH709)
86plusmn14(51ndash117
)122plusmn55(58ndash383)
6plusmn1(3ndash10)
11plusmn8(3ndash33)
51139plusmn1169(49967ndash5340
2)44plusmn05(4-5)3067plusmn725(1266ndash4
838)
Uberla
ndiaM
G
6 Advances in Zoology
60∘W 50
∘W 40∘W
0∘
10∘S
20∘S
30∘S
0 400
(km)
PA MA
PICE
4
5
6
MT
32
1
1
7
8
910
11
12
SP
GO
N
Figure 1 Geographical variation in the advertisement calls (oscillograms) of Pseudopaludicola mystacalis from twelve localities in sevenBrazilian states Para (PA) Primavera (1) Ceara (CE) Itapipoca (2) Taıba (3)Maranhao (MA) Balsas (4) Piauı (PI) Brejo do Piauı (5) Goias(GO) Uruacu (6) Mato Grosso (MT) Cuiaba (7) Chapada dos Guimaraes (8) Nossa Senhora do Livramento (9) Pocone (10) Caceres (11)Sao Paulo (SP) Icem (12) Total time of each oscillogram corresponds to 02 s
(Figure 3(c)) and higher loadings corresponded to note rate(385) internote interval (295) and note duration (221) Nodistinct groups were formed along the first function axis ofthe DFA
32 Taxonomic Status of Pseudopaludicola serrana Toledo2010 Advertisement calls of Pseudopaludicola serranarecorded at the type-locality (Brumadinho Minas Gerais)and nearly 120 km southwestwards at Serra do LenheiroMinas Gerais were similar to those of topotypes of P
murundu and distinct from topotypes of P saltica bothin spectral and temporal parameters (Figures 4 and 5)The intraspecific variation in bioacoustic parameters ofP murundu and P serrana presented below is based oncalls from topotypical specimens and on calls recorded inadditional localities listed in Appendix B
Advertisement calls of P serranawere composed of seriesof pulsed notes with nonconcatenated pulses Each note con-sisted of 36plusmn06 (range 2ndash5) pulses Mean note duration was82 plusmn 58ms (26ndash131) emitted on average at intervals of 167 plusmn58ms (63ndash288) Mean duration of each pulse was 9 plusmn 3ms
Advances in Zoology 7
Taiba(CE)
Uruaccedilu(GO)
BBuriti(PI)
C aceres
Livramento (MT)(MT)
(MT)(MT)
(MT) Pocon eCGuimaraes
Cuiab a Itapipoca(CE)
Primavera(PA)
Ic em(SP) Balsas
(MA)
(kH
z)8
7
6
5
4
3
2
1
(s)02 04 06 08 1 12 14 16 18 2 22 24 26 28 3 32 34 36 38
ı
Figure 2 Spectrograms (DFT size = 512 samples) of the advertisement calls of Pseudopaludicola mystacalis from twelve localities (two notesfor each locality) in seven Brazilian states (CE Ceara GO Goias MA Maranhao MT Mato Grosso PA Para PI Piauı SP Sao Paulo)
(2ndash18) Interpulse intervals were 16 plusmn 7ms long (4ndash41) Meanfrequency ranged from 40196 plusmn 453Hz to 70986 plusmn 312Hzand mean dominant frequency was 56251 plusmn 212Hz (5168ndash60293) Advertisement calls of Pmurunduwere composed ofseries of pulsed noteswith nonconcatenated pulses Each noteconsisted of 34 plusmn 06 (range 2ndash5) pulses Mean note durationwas 92 plusmn 18ms (33ndash143) emitted on average at intervals of121 plusmn 30ms (69ndash247) Mean duration of each pulse was 10 plusmn3ms (4ndash18) Interpulse intervals were 24plusmn8ms (5ndash54) Meanfrequency ranged from 36285 plusmn 513Hz to 73301 plusmn 355Hzand mean dominant frequency was 55901 plusmn 176Hz (4875ndash62016Hz)
A discriminant function analysis (DFA)withmorphome-tric data revealed that P serrana and P murundu overlappedalong the first function (DF1) ofDFAwhich explained 98ofthe total variation (Figure 6(a)) While the DFA did not sep-arate P serrana from P murundu both were separated froma third species (Pseudopaludicola saltica) whose individualsalso have long hindlimbs Higher loadings corresponded toeye diameter (121) tarsus length (75) and tibia length (46)DFA from bioacoustic data also separated Pseudopaludicolasaltica from P murundu and P serrana (Figure 6(b))The firstfunction (DF1) of DFA explained 99 of the total variationand higher loadings corresponded to dominant frequency(641) and number of pulses per note (61)
DFAofmorphometricmeasurements using all specimensassigned 100 of the individuals of Pseudopaludicola saltica86 of the individuals of P serrana and only 16 of theindividuals of P murundu to the correct species (Table 5)DFA of bioacoustic variables using all recorded males cor-rectly assigned 89 of the specimens of P saltica 83 of thespecimens of P murundu and 40 of P serrana (Table 5) Incontrast DFA with both morphometric and bioacoustic datausing specimens ofP saltica and amixed sample of specimensattributable to either P murundu or P serrana assigned 100of these latter to a single taxon
The overall similarity in morphology and general struc-ture of the call of P murundu and P serrana evidenced bythe results of DFA with 12 morphometric and six bioacous-tic variables strongly support the rejection of the specificstatus of Pseudopaludicola serrana here considered to be a
junior synonym of Pseudopaludicola murundu Geographi-cal distribution of Pseudopaludicola murundu as presentlyrecognized is not anymore restricted to its type-locality [16]but includes instead twelve distinct localities in southeasternBrazil in the states of Minas Gerais and Sao Paulo (Figure 7)
4 Discussion
41 Geographical Variation in Pseudopaludicola mystacalis(Cope 1887) Among the 18 valid species of Pseudopalu-dicola P mystacalis is currently the one with the mostwidespread distribution range Extent of occurrence in Brazilis nearly two million square kilometers encompassing areasin three different ecoregions along all the ldquodiagonal of openformationsrdquo from South America [23] Caatinga Cerradoand Pantanal It is also found in areas of Chaco in Argentina[24] and Paraguay [25] Although plausible the occurrence inBolivian Chaco was based on material that morphologicallyand bioacoustically would correspond to P ameghini [12 26]Habitats where individuals of this species were found includeldquorestingardquo [10 present study] ldquocampo sujordquo in elevatedplateaus of theCerradoDomain and seasonally floodedfieldsin the Pantanal lowlands [8]
Advertisement calls of Pseudopaludicola mystacalis fromdifferent Brazilian localities are composed of series of noteswith concatenated pulses Maximum variation in dominantfrequency of the calls of all specimens analyzed is 8613Hz(from 44789Hz in Cuiaba Mato Grosso to 53402Hz inBalsas Maranhao Table 3) without any evident latitudinalor longitudinal trend Dominant frequency in the mostdistant known locations (Primavera state of Para and Icemstate of Sao Paulo) varied by 3721 Hz Considering subsetsof populations from Brazilian Northeast (states of CearaMaranhao and Piauı) and from Brazilian Midwest (statesof Mato Grosso and Goias) maximum interpopulationalvariation in dominant frequency is 646Hz and 7752Hzrespectively Maximum intrapopulational variation in dom-inant frequency evaluated for four localities in the lowerportion of the speciesrsquo range (Caceres Cuiaba Nossa Senhorado Livramento and Pocone state ofMatoGrosso) is 5168Hzin Cuiaba (see Table 3 and [8])
8 Advances in Zoology
3
2
1
0
minus1
minus2
210minus1minus2minus3
DF2
(37
)
DF1 (63)
(a)
3
2
1
0
minus1
minus2
minus3
3210minus1minus2minus3minus4
DF2
(15
)
DF1 (85)
(b)
2
1
0
minus1
210minus1minus2
DF1 (79)
DF2
(21
)
Chapada dos Guimaraes-MTCuiab a-MTNS Livramento-MTPorto Estrela-MTC aceres-MTBarra do Garccedilas-MTPocon e-MTUruaccedilu-GO
Alto Alegre-SP
Primavera-PAItapipoca-CETaBalsas-MABrejo do Piauı-PIacute
ıba-CE
Ic em-SP
(c)
Figure 3 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of 101 males (a) 37 females (b)and six bioacoustic variables (c) of Pseudopaludicola mystacalis from 15 different localities in Brazil
Maximum variation in temporal variables (notes perminute and number of pulses) of the calls of all specimensanalyzed is 2136 notesmin and 8 pulsesnote In the mostdistant known locations the difference in the number of notesper minute and in the number of pulses is 1003 notesmin
and 6 pulsesnote respectively Considering subsets of pop-ulations from Brazilian Northeast and Brazilian Midwestmaximum interpopulational variation is 1146 notesmin and1335 notesmin respectively There are 7 pulsesnote in callsfrom populations of both areas Maximum intrapopulational
Advances in Zoology 9
Pseudopaludicola serrana Pseudopaludicola murundu Pseudopaludicola saltica
05 1 15 2 25 3 35 4 45 5
A B C D E F G H I(k
Hz)
8
7
6
5
4
3
2
1
(s)
Figure 4 Spectrograms (DFT size = 512 samples two notes for each locality) of advertisement calls of Pseudopaludicola serrana (AndashC) andP murundu (DndashF) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais-Uberlandia (G) state of MatoGrosso-Chapada dos Guimaraes (type-locality H) and Porto Estrela (I)
Note Pulses
(a) (b)
(c) (d)
(e) (f)
(g) (h)
Figure 5 Oscillograms of advertisement calls of Pseudopaludicola serrana (a)-(b) and P murundu (c)ndash(e) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais Uberlandia (f) state of Mato Grosso Chapada dos Guimaraes (type-locality (g))and Porto Estrela (h) Total time of each oscillogram corresponds to 05 s
10 Advances in Zoology
4
2
0
minus2
minus4
6420minus2minus4
DF2
(2
)
DF1 (98)
(a)
4
2
0
minus2
minus4
6420minus2minus4
DF2
(1
)
DF1 (99)
(b)
Figure 6 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of males (a) and six bioacousticvariables (b) of Pseudopaludicola murundu (open circles) P saltica (triangles) and P serrana (closed circles)
Elevation (m)
0
(km)
minus155ndash350351ndash700701ndash1050
1050ndash14001401ndash1750
300
N
1
2
3
4
5
6 78
91011
12
13
Figure 7 Geographical distribution of Pseudopaludicola murundu(circles) and P saltica (triangles) in southeastern Brazil state of SaoPaulomdashRioClaro (type locality (1)) andCampinas (2) state ofMinasGeraismdashPocos de Caldas (3) Alpinopolis (4) (see [17]) Sao Roquede Minas (5) Sao Joao Del Rei (6) Mariana (7) Ouro Branco (8)Itabirito (9) Brumadinho (10) Lavras Novas (11) Botumirim (12)and Uberlandia (13)
variation in the number of notes per minute and in thenumber of pulses in four localities from the state of MatoGrosso is 81 notesmin in Cuiaba and 5 pulsesnote in Cuiabaand Nossa Senhora do Livramento (see Table 3 and [8])Mean note duration does not differ significantly in all theexamined calls (Table 3 119865 = 49 df = 2 119875 = 003)
Table 5 Summary of the number of male specimens correctlyclassified as Pseudopaludicolamurundu P saltica or P serrana usingdiscriminant function analysis of 12 morphometric measurementsand seven bioacoustic variables
Morphometric measurementsTrue group
P murundu P saltica P serranaP murundu 1 0 5P saltica 0 39 0P serrana 3 0 19Total number 6 39 22 16 100 86
Bioacoustic variablesTrue group
P murundu P saltica P serranaP murundu 5 0 1P saltica 0 8 1P serrana 3 0 2Total number 6 9 5 83 889 40
Acoustic analysis of geographical variation in specieswith an extent of occurrence of the magnitude seen inP mystacalis sometimes reveals cryptic taxa being treatedunder a single name However this was not the case in Pmystacalis a taxon that remained erroneously characterizedand poorly recognized in the literature until recently [8] Ourresults reveal a relatively small variation in morphologicaland acoustical traits of P mystacalis and allow confirming thepresence of the species in a wide geographical area along theBrazilian open ecosystems
Advances in Zoology 11
Table 6 Ratios of selected measurements (in mm) of males of Pseudopaludicola murundu P salticaand P serrana Values are presented asmean plusmn standard deviation119873 = number of specimens analyzed
HLSVL HWSVL HLHW HALSVL FLSVL THLSVL TLSVLP serrana (119873 = 21) 040 plusmn 003 036 plusmn 002 110 plusmn 006 027 plusmn 002 061 plusmn 004 056 plusmn 003 070 plusmn 003
P murundu (119873 = 5) 039 plusmn 004 035 plusmn 003 111 plusmn 009 027 plusmn 001 066 plusmn 002 056 plusmn 002 070 plusmn 003
P saltica (119873 = 44) 041 plusmn 004 038 plusmn 003 109 plusmn 011 026 plusmn 003 068 plusmn 006 055 plusmn 005 073 plusmn 005
HAL hand length HL head length HW head width FL foot length SVL snout-vent length THL thigh length TL tibia length
42 Taxonomic Status of Pseudopaludicola serrana Toledo2010 When describing P serrana Toledo [15] used asmorphological characteristics separating the three speciesbelonging to the P saltica group the aspect (relative size andcoloration) of nuptial pads in the external part of finger I andaspect of the vocal sac Such characteristics allow differingP serrana and P murundu from P saltica but do not allowdiffering P serrana from P murundu [15] Previously Haddadand Cardoso [17] had called attention to the fact that nuptialpads were more developed in specimens of P saltica from thetype-locality (Chapada do Guimaraes Mato Grosso) than inspecimens collected and recorded in localities in the statesof Minas Gerais and Sao Paulo In the same article Haddadand Cardoso [17] also presented a spectrogram of the callof a specimen from Campinas Sao Paulo Based on suchreported morphological evidence and acoustic parameterswe here argue that specimens from Minas Gerais and SaoPaulo attributed to P saltica in Haddad and Cardoso [17] infact correspond to P murundu
The only external morphological characteristic used byToledo [15] to differ P serrana from P murunduwas a shorterhead lengthheadwidth ratio (HLHW= 097plusmn006 in the fiveindividuals ofP serrana evaluated 111plusmn007 in 11 individualsof P murundu) After having analyzed a higher number ofspecimens attributed to P serrana (119873 = 21) we found thatHLHW (110 plusmn 006 see Table 6) in this sample does notdiffer from the values presented in the original descriptionand confirmed herein for P murundu
The description of P serrana was also based on physicalcharacteristics of its advertisement calls [15] However theoriginal dataset is relatively low 12 notes of a single maleof P saltica 14 notes of 2 males of P murundu and 15notes of 3 males of P serrana were analyzed and comparedOnly one out of four acoustic variables (pulse duration) wasconsidered diagnostic for the new species Toledo [15] alsoshowed that dominant frequency range of P serrana wascompletely nested within the dominant frequency range of Pmurundu However when later proposing the synonymiza-tion of Pseudopaludicola riopiedadensis Mercadal de Bar-rio and Barrio 1994 to Pseudopaludicola ternetzi Miranda-Ribeiro 1937 Cardozo and Toledo [5] based their decision onldquoseveral important overlapsrdquo including dominant frequencyranges between the two species Indeed our data showedthat dominant frequency contributed to higher loadingsto separate species in the P saltica group Nonoverlappingdominant frequencies would therefore be expected betweenrelated but distinct species of Pseudopaludicola
Bioacoustic data have proven to be useful for uncoveringmorphologically cryptic species in the genus Pseudopaludi-cola [4ndash9 15 16] Advertisement calls of species in this genusmight be divided into three distinct groups according to typeof notes nonpulsed notes notes with concatenated pulsesand noteswith nonconcatenated pulses [7] Each groupmightbe diagnosed by temporal (pulses per note note and pulseduration internotes and interpulses intervals note rate andpulse rate) and spectral variables (dominant frequency andharmonics) which in combination allow characterizing allthe species for which calls were already analyzed except forP serrana and P murundu As evidenced by the recent syn-onymization of Pseudopaludicola riopiedadensis to P ternetzi[15] and reinforced herein by the proposed synonymizationof P serrana to P murundu morphologically similar speciesof Pseudopaludicola presenting the same type of note and anoverlap in their spectral acoustic variables are expected torepresent the same taxon Therefore no arguments remainto consider P serrana as a distinct species from P murunduand the former must be considered as a junior synonym of Pmurundu
5 Conclusions
We here report on the variation in morphometric charactersand variation in bioacoustic variables of the advertisementcalls in fifteen Brazilian populations of Pseudopaludicolamys-tacalis Although limited our sample evidenced no statisticaldifferences in any of the evaluated attributes and allowed usto confirm that this species is widely distributed in BrazilMorphometric and bioacoustic data did not differ also inpopulations currently attributed to Pseudopaludicola serranaand Pseudopaludicola murundu and the former taxon ishere considered as a junior synonym of P murundu Thedata in the present work aims at contributing to a betterunderstanding of the diversity and distribution patterns inthe genus Pseudopaludicola
Appendices
A Voucher Specimens Examined
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality 22∘1910158405210158401015840S 47∘4210158405610158401015840W)-F UFMT 18454MUFMT 18395-6 UFMT 18455-7
Pseudopaludicola mystacalis Brazil Para Primavera(00∘5710158402210158401015840S 47∘0710158401210158401015840W)-M UFMT 11651 UFMT 11827
12 Advances in Zoology
UFMT 11833 UFMT 11836 UFMT 11839 Goias Uruacu(14∘3110158403510158401015840S 49∘0710158405410158401015840W)-F UFMT 18397-400 UFMT18458-9 M UFMT 18401-15 UFMT 18458-64 Mato GrossoBarra do Garcas (15∘3110158405710158401015840S 52∘1410158401010158401015840W)-M UFMT11097 UFMT 11307 UFMT 11319 UFMT 11324 Caceres(16∘1710158405910158401015840S 58∘0910158400910158401015840W)-F UFMT 5906 UFMT 5950UFMT 5955 UFMT 5962 UFMT 9152 UFMT 10445UFMT 10448 UFMT 13669 M UFMT 10451-2 UFMT10455 UFMT 10458 UFMT 10466 UFMT 10495 UFMT10506 UFMT 10508 UFMT 13670 Chapada dos Guimaraes(type-locality 14∘5010158403410158401015840S 55∘2310158401010158401015840W)-F UFMT 8109 MUFMT 487 UFMT 817 UFMT 820 UFMT 12890 Cuiaba(15∘3910158403310158401015840S 55∘5610158403010158401015840W)-M UFMT 15980 UFMT 2426UFMT 2430 UFMT 2432 UFMT 2434-7 UFMT 2439UFMT 7399 UFMT 7653 UFMT 8177-8 UFMT 8180UFMT 8182 UFMT 8184-5 UFMT 13671 Nossa Senhorado Livramento (16∘2110158405810158401015840S 56∘1810158403310158401015840W)-F UFMT 18465UFMT 352 UFMT 6436 UFMT 6466-7 UFMT 6488UFMT 6511 M UFMT 4343 UFMT 6487 UFMT 6491UFMT6498UFMT6515Pocone (16∘3010158405810158401015840S 56∘4410158405310158401015840W)-M UFMT 348-50 UFMT 889 UFMT 4316 UFMT 4318UFMT 4321 UFMT 13672 and Porto Estrela (15∘3510158400510158401015840S57∘1310158402010158401015840W)-F UFMT 18466-7 UFMT 138 UFMT 13482M UFMT 18468-9 UFMT 402 UFMT 2200 UFMT 11346Sao Paulo Icem (20∘2010158403110158401015840S 49∘1110158404210158401015840W)-F UFMT 18421UFMT 18470-2 M UFMT 18422-3 UFMT 18473 and AltoAlegre (21∘3310158402010158401015840S 50∘1310158402210158401015840W)-F UFMT 18474-5 UFMT18479 MUFMT 18476-8 UFMT 18480-6
Pseudopaludicola saltica Brazil Mato Grosso Chapadados Guimaraes (type-locality 15∘2310158400910158401015840S 55∘5010158402410158401015840W)-MUFMT 482 UFMT 819 UFMT 821 UFMT 823 UFMT 1433-5 UFMT 1437-41 UFMT 2873 UFMT 2877 UFMT 2880-1F UFMT 1442 Cuiaba M UFMT 270 UFMT 473 UFMT476 UFMT 13657-68 F UFMT 13655-6) Nova Lacerda (MUFMT 13499-501) Porto Estrela Estacao Ecologica da Serradas Araras (M UFMT 561) and Vila Bela da SantıssimaTrindade (M UFMT 4082 UFMT 4112 UFMT 4123 UFMT4147 UFMT4153 UFMT4157 UFMT4172)MatoGrosso doSul Sonora (M UFMT 1147 UFMT 1195)
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho (type-locality 20∘0610158403210158401015840S 43∘5810158405310158401015840W)-F MCNAM 3675 MUFMT 18424 UFMT 18451 MCNAM 3677-8 MCNAM3680 Itabirito (20∘1310158402910158401015840S 43∘4810158404910158401015840W)-F MCNAM14620-1 M MCNAM 14625 Lavras Novas (20∘2810158405710158401015840S43∘3010158405210158401015840W)-F MCNAM 3694 M MCNAM 3695MCNAM 3690 Mariana (20∘0910158401210158401015840S 43∘3010158400210158401015840W)-FMCNAM 6465 M MCNAM 6457 MCNAM 6461-2 OuroBranco (20∘3010158401610158401015840S 43∘4210158400410158401015840W)-M MCNAM 6559 SaoJoao Del Rei (21∘0810158402510158401015840S 44∘1710158403110158401015840W)-M UFMT 18425-6UFMT 18452-3 and Botumirim (16∘4410158401310158401015840S 42∘3410158402910158401015840W)-FMCNAM 6713 M MCNAM 6832 MCNAM 6834 MCNAM6636 MCNAM 6642-3
B Analyzed Sound Files
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality) LH 676 no voucher specimen LH 677 call
fromUFMT 18455 LH 678 call fromUFMT 18395 and FNJV12976 no voucher specimen Minas Gerais Sao Roque deMinas (20∘1310158402010158401015840S 46∘2710158402410158401015840W) FNJV 4575 no voucherspecimen and Pocos de Caldas (21∘5510158400410158401015840S 46∘3410158400210158401015840W)FNJV 4576 no voucher specimen
Pseudopaludicola mystacalis Brazil Ceara Itapipoca(03∘2410158405810158401015840S 39∘4110158403110158401015840W) LH 655 no voucher specimenTaiba (03∘2510158404410158401015840S 38∘5710158404310158401015840W) LH 658 no voucher spec-imen Goias Uruacu LH 639 call from UFMT 18410) MatoGrosso Chapada dos Guimaraes (type-locality) LH 13A-05no voucher specimen) Caceres LH 47A-04 call fromUFMT10451 Cuiaba LH 14A-01 call from UFMT 2426 LH 14A-02 call from UFMT 2424 Pocone LH 01A-01 call fromUFMT 4321 and Nossa Senhora do Livramento LH 04A-10 call from UFMT 4330 Maranhao Balsa (07∘2810158404910158401015840S46∘0310158401910158401015840W) LH 284 no voucher specimen Piauı Brejo doPiauı (08∘1110158405010158401015840S 42∘4910158405910158401015840W) LH 184 call from UFMT11202 Para Primavera LH 352 call from UFMT 11836 SaoPaulo Icem LH 701 call from UFMT 18423
Pseudopaludicola saltica BrazilMatoGrossoCuiaba LH13A-01 call fromUFMT 8187Nova Lacerda LH 42A-06 callfrom UFMT 13499 LH 42A-07 call from UFMT 13500 andPorto Estrela LH 12 no voucher specimen LH 13 call fromUFMT 13678 LH 14 call fromUFMT 16423 LH 16 call fromUFMT 16417 LH 17 call from UFMT 16414 and LH 18 callfrom UFMT 16385 Minas Gerais Uberlandia (18∘5810158403010158401015840S48∘1710158402610158401015840W) LH 709 no voucher specimen
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho LH 673call from UFMT 18451 LH 674 no voucher specimen andSao Joao Del Rei LH 675 call from UFMT 18426 and FNJV12879-80 no voucher specimen
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Special thanks go to Felipe Franco Curcio Diva MariaBorges-Nojosa and Luciana Barreto Nascimento for allow-ing access to the material under their care at ldquoColecaoZoologica de Vertebrados da Universidade Federal de MatoGrossordquo (UFMT) ldquoColecao Herpetologica da UniversidadeFederal do Cearardquo (UFC) and ldquoMuseu de Ciencias Naturaisrdquo(MCNAM Belo Horizonte Minas Gerais) respectively toAdao J Cardoso (in memoriam) and Luis F Toledo for therecordings and for allowing access respectively to bioa-coustic samples deposited at ldquoFonoteca Neotropical JacquesVielliardrdquo (FNJV) to the CNPq project ldquoRede de pesquisa emanfıbios e repteis de ecossistemas nao florestais brasileirosrdquo(Process no 5633522010-8) for logistical support to VivianUhlig (RANICMBio) for estimates of extent of occurrenceAndre Pansonato thanks ldquoCoordenacao de Aperfeicoamentode Pessoal de Nivel Superiorrdquo (CAPES) for a PhD scholar-ship and Christine Strussmann thanks CNPq for a researchfellowship (Process no 3095412012-3)
Advances in Zoology 13
References
[1] K D Wells The Ecology amp Behavior of Amphibians TheUniversity of Chicago Chicago Ill USA 2007
[2] M Vences M Gehara J Kohler and F Glaw ldquoDescription of anewMalagasy treefrog (Boophis) occurring syntopically with itssister species and a plea for studies on non-allopatric speciationin tropical amphibiansrdquo Amphibia Reptilia vol 33 no 3-4 pp503ndash520 2012
[3] I De La Riva R Marquez and J Bosch ldquoDescription ofthe advertisement calls of some South American Hylidae(Amphibia Anura) taxonomic and methodological conse-quencesrdquo Bonner Zoologische Beitrage vol 47 pp 175ndash185 1997
[4] F S de Andrade and T R de Carvalho ldquoA new species of Pseu-dopaludicola Miranda-Ribeiro (Leiuperinae LeptodactylidaeAnura) from the Cerrado of southeastern Brazilrdquo Zootaxa vol3608 no 5 pp 389ndash397 2013
[5] D Cardozo and L F Toledo ldquoTaxonomic status of Pseudopalu-dicola riopiedadensis Mercadal de Barrio and Barrio 1994(Anura Leptodactylidae Leiuperinae)rdquo Zootaxa vol 3734 pp571ndash582 2013
[6] T R de Carvalho ldquoA new species of PseudopaludicolaMiranda-Ribeiro (Leiuperinae Leptodactylidae Anura) from the Cer-rado of southeastern Brazil with a distinctive advertisement callpatternrdquo Zootaxa no 3328 pp 47ndash54 2012
[7] F M Magalhaes D Loebmann M N C Kokubum C F BHaddad and A A Garda ldquoA new species of Pseudopaludi-cola (Anura Leptodactylidae Leiuperinae) from NortheasternBrazilrdquo Herpetologica vol 70 pp 77ndash88 2014
[8] A Pansonato C Strussmann J R Mudrek and I A Mar-tins ldquoMorphometric and bioacoustic data on three species ofPseudopaludicola Miranda-Ribeiro 1926 (Anura Leptodactyl-idae Leiuperinae) described from Chapada dos GuimaraesMato Grosso Brazil with the revalidation of Pseudopaludicolaameghini (Cope 1887)rdquo Zootaxa vol 3620 no 1 pp 147ndash1622013
[9] I J Roberto D Cardozo and R W Avila ldquoA new speciesof Pseudopaludicola (Anura Leiuperidae) from Western PiauıState Northeast Brazilrdquo Zootaxa vol 3636 no 2 pp 348ndash3602013
[10] S B Barreto M S Tinoco D Couto-Ferreira and H CBrowne-Ribeiro ldquoDistribuicao de Pseudopaludicola aff falcipes(Anura Leiuperidae) na restinga do litoral norte da BahiaBrasilrdquoRevista Latino-Americana de Conservacao vol 2 pp 27ndash36 2012
[11] E R Favero A C P Veiga-Menoncello D C Rossa-Feres et alldquoIntrageneric karyotypic variation in Pseudopaludicola (AnuraLeiuperidae) and its taxonomic relatednessrdquo Zoological Studiesvol 50 no 6 pp 826ndash836 2011
[12] M Jansen R Bloch A Schulze andM Pfenninger ldquoIntegrativeinventory of Boliviarsquos lowland anurans reveals hidden diversityrdquoZoologica Scripta vol 40 no 6 pp 567ndash583 2011
[13] C P D Prado M Uetanabaro and C F B Haddad ldquoBreed-ing activity patterns reproductive modes and habitat use byanurans (Amphibia) in a seasonal environment in the PantanalBrazilrdquo Amphibia Reptilia vol 26 no 2 pp 211ndash221 2005
[14] R A Silva I A Martins and D C Rossa-Feres ldquoBioacustica esıtio de vocalizacao em taxocenoses de anfıbios de area abertano Noroeste Paulistardquo Biota Neotropica vol 8 pp 123ndash1342008
[15] L F Toledo ldquoDescription of a new species of PseudopaludicolaMiranda-Ribeiro 1926 from the state of Sao Paulo SoutheasternBrazil (Anura Leiuperidae)rdquoZootaxa no 2681 pp 47ndash56 2010
[16] L F Toledo S Siqueira T CDuarte A C P Veiga-MenoncelloS M Recco-Pimentel and C F B Haddad ldquoDescription of anew species of Pseudopaludicola Miranda-Ribeiro 1926 fromthe state of Sao Paulo Southeastern Brazil (Anura Leiuperi-dae)rdquo Zootaxa no 2496 pp 38ndash48 2010
[17] C F B Haddad and A J Cardoso ldquoTaxonomia de tres especiesde Pseudopaludicola (Anura Leptodactylidae)rdquo Papeis Avulsosde Zoologia vol 36 pp 287ndash300 1987
[18] T C Duarte A C P Veiga-Menoncello J F R Lima et alldquoChromosome analysis in Pseudopaludicola (Anura Leiuperi-dae) with description of sex chromosomes XXXY in P salticardquoHereditas vol 147 no 2 pp 43ndash52 2010
[19] A C P Veiga-Menoncello L B Lourenco C Strussmannet al ldquoA phylogenetic analysis of Pseudopaludicola (Anura)providing evidence of progressive chromosome reductionrdquoZoologica Scripta vol 43 no 3 pp 261ndash272 2014
[20] W R Heyer A S Rand C A G Cruz O L Peixoto and CE Nelson ldquoFrogs of Boraceiardquo Arquivos de Zoologia vol 31 pp231ndash410 1990
[21] W E Duellman The Hylid Frogs of Middle America vol 1 ofMonograph of the Museum of Natural History of University ofKansas 1970
[22] R Development Core Team The R Project for Statistical Com-puting Vienna Austria 2013 httpwwwr-projectorg
[23] P E Vanzolini ldquoEcological and geographical distribution oflizards in Pernambuco Northeastern Brasil (Sauria)rdquo PapeisAvulsos de Zoologia vol 18 no 4 pp 61ndash90 1974
[24] J M Cei ldquoAmphibians of Argentinardquo Monitore ZoologicoItaliano Nuova Serie Monografia vol 2 pp 1ndash609 1980
[25] F Brusquetti and E O Lavilla ldquoLista comentada de los anfibiosde ParaguayrdquoCuadernos deHerpetologıa vol 20 no 2 pp 3ndash792006
[26] I De La Riva J Kohler S Lotters and S Reichle ldquoTenyears of research on Bolivian amphibians updated checklistdistribution taxonomic problems literature and iconographyrdquoRevista Espanola Herpetologica vol 14 pp 19ndash164 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
4 Advances in Zoology
Table 3 Measurements of bioacoustic variables of the advertisement calls of specimens of Pseudopaludicola mystacalis from 12 localities inseven Brazilian states (CE Ceara GO Goias MA Maranhao MT Mato Grosso PA Para PI Piauı SP Sao Paulo) Values are presented asmean plusmn standard deviation (minimumndashmaximum)119873 number of notes analyzed
LocalitymdashState Air temp Noteduration (ms)
Internoteinterval (ms)
Pulses pernote
Pulseduration (ms)
Dominantfrequency (Hz)
Notesmin(mean)
PoconemdashMT (119873 = 30) 256∘C 40 plusmn 5
(30ndash50)80 plusmn 10
(60ndash100)16 plusmn 12
(14ndash18)2 plusmn 03
(1-2)46842 plusmn 1157
(4522ndash49096)5111
NS LivramentomdashMT (119873 = 25) 252∘C 40 plusmn 4
(40ndash50)70 plusmn 30
(50ndash200)17 plusmn 10
(14ndash19)2 plusmn 03
(1-2)48114 plusmn 563
(47373ndash49096)5064
C GuimaraesmdashMT (119873 = 110) 263∘C 40 plusmn 4
(30ndash50)60 plusmn 10
(40ndash100)16 plusmn 08
(14ndash17)2 plusmn 04
(1-2)49624 plusmn 1815
(46512ndash52541)5769
CuiabamdashMT (119873 = 25) 26∘C 50 plusmn 4
(30ndash50)90 plusmn 10
(60ndash100)14 plusmn 08
(12ndash16)2 plusmn 04
(1ndash3)47752 plusmn 828
(46512ndash49096)4433
CuiabamdashMT (119873 = 25) 26∘C 45 plusmn 4
(30ndash50)80 plusmn 30
(50ndash200)16 plusmn 10
(13ndash18)2 plusmn 03
(1-2)48372 plusmn 150
(44789ndash49957)5243
CaceresmdashMT (119873 = 25) 26∘C 50 plusmn 3
(40ndash50)60 plusmn 50
(50ndash70)16 plusmn 10
(14ndash18)2 plusmn 03
(1-2)4901 plusmn 512
(47373ndash49957)5389
BalsasmdashMA (119873 = 30) 265∘C 40 plusmn 2
(37ndash45)80 plusmn 5
(70ndash90)16 plusmn 10
(14ndash18)2 plusmn 04
(1-2)507609 plusmn 20568
(47804ndash53402)5137
IcemmdashSP (119873 = 28) 23∘C 50 plusmn 5
(50ndash60)110 plusmn 7
(100ndash150)17 plusmn 17
(14ndash20)2 plusmn 04
(1-2)48722 plusmn 799
(47373ndash49742)3633
ItapipocamdashCE (119873 = 30) mdash 50 plusmn 3
(40ndash50)90 plusmn 10
(70ndash130)16 plusmn 12
(14ndash18)2 plusmn 04
(1-2)51282 plusmn 981
(47804ndash5211)4207
TaıbamdashCE (119873 = 30) mdash 40 plusmn 2
(40ndash50)70 plusmn 2
(60ndash70)16plusmn11(13ndash18)
2plusmn05(1ndash3)
47952plusmn852(46942ndash49526)
5353
Brejo do BuritimdashPI (119873 = 30) 27∘C 50 plusmn 1
(45ndash50)90 plusmn 20
(60ndash140)19 plusmn 06
(18ndash20) 2 486075 plusmn 3148
(48234ndash49096)4296
PrimaveramdashPA (119873 = 30) 255∘C 50 plusmn 2
(40ndash50)80 plusmn 5
(70ndash100)18plusmn12(16ndash20)
2plusmn05(1-2)
50406plusmn456(49219ndash51094)
4637
UruacumdashGO (119873 = 26) 245∘C 50plusmn2(40ndash50)
60plusmn5(50ndash80)
16plusmn12(14ndash18)
2 plusmn 05
(1-2)46334 plusmn 866
(4500ndash49688)5435
Mean plusmn SD 50 plusmn 4(30ndash60)
80 plusmn 10(40ndash200)
16 plusmn 17(12ndash20)
2 plusmn 04(1ndash3)
48874 plusmn 1495(44789ndash53402)
4901plusmn611(3633ndash5769)
notes perminute Dominant frequency (note peak frequencyHz) was obtained from the spectrogram Terminology forbioacoustic variables follows Magalhaes et al [7] Pansonatoet al [8] and Heyer et al [20] Vocalizations are archivedin the ldquoBanco de Registros Bioacusticosrdquo and housed at theldquoLaboratorio de Herpetologia do Instituto de Biociencias daUniversidade Federal de Mato Grossordquo (LH Cuiaba MatoGrosso)
Discriminant function analyses (DFA) were conducted inorder to evidence the set of morphometric and bioacousticvariables that mostly distinguish between the species ofPseudopaludicola compared herein DFA were performed oncorrelation matrices from 12 log-transformed morphometricand six bioacoustic variables using R platform version 301[22] Bioacoustic comparisons through the DFA were per-formed using mean individual values
3 Results
31 Geographical Variation in Pseudopaludicola mystacalis(Cope 1887) Based on morphology and bioacoustics Pseu-dopaludicola mystacalis was positively identified in fifteenlocalities (Figure 1) from seven Brazilian states Ceara Goias
Maranhao Mato Grosso Para Piauı and Sao Paulo Theadvertisement calls of Pseudopaludicola mystacalis along itsdistribution range in Brazil (Figures 1 and 2) consistedof series composed of 9ndash229 notes with 16 plusmn 17 (12ndash20)concatenated pulses (ie no interpulse intervals) Mean noterepetition rate was 4901 plusmn 611 notesmin (3633ndash5769)mean duration of each note was 50 plusmn 4ms (30ndash60) averageinternote interval varied from 80 plusmn 10ms (40ndash200) Meanpulse duration was 2 plusmn 04ms (1ndash3) Frequency ranged from26862Hz to 73433Hz and dominant frequency ranged from44789 to 53402Hz (Table 3)
Discriminant function analysis (DFA) with our dataon P mystacalis did not group localities neither regardingmorphometric characters (males and females) nor regardingbioacoustic variables The first function (DF1) of DFA withmorphometric data explained 63 of the variation amongmales of different populations (Figure 3(a)) and higherloadings corresponded to thigh length (105) hand length(98) and foot length (84) The DF1 explained 85 of thevariation among females (Figure 3(b)) and higher loadingscorresponded to hand length (123) foot length (107) andsnout-vent length (88) The DF1 of DFA with bioacousticvariables explained 79 of the total variation in our sample
Advances in Zoology 5
Table4
Measurementsof
bioacoustic
varia
bles
oftheadvertise
mentc
allsof
specim
enso
fPseud
opalud
icola
murun
duPsalticaandPserranaVa
lues
arepresentedas
meanplusmnsta
ndard
deviation(m
inim
umndashm
axim
um)
Species
(vou
cher
record)
Noted
uration(m
s)Internoteinterval(ms)
Pulse
duratio
n(m
s)Interpulsesinterval(ms)
Dom
inantfrequ
ency
(Hz)
Pulse
sno
teNotesm
inMun
icipality
state
Pmurun
du(LH676)
80plusmn12(58ndash105)
100plusmn15(69ndash
141)
8plusmn2(4ndash12)
26plusmn7(7ndash4
0)56007plusmn2043(5168ndash5857)33plusmn07(2ndash5)3489plusmn219(3145ndash3704)
RioClaroSP
Pmurun
du(LH677)
94plusmn11(49ndash
114)
98plusmn16(70ndash
140)
13plusmn2(9ndash17)
23plusmn9(6ndash39)
55799plusmn1502(52541ndash5857)29plusmn02(2-3)3172plusmn176(2956ndash3419)
RioClaroSP
Pmurun
du(LH678)
89plusmn13(33ndash104)
107plusmn12(89ndash
137)
9plusmn2(5ndash17)
20plusmn8(8ndash4
6)57259plusmn1297(53402ndash59001)37plusmn05(2ndash4
)3087plusmn139(2926ndash3264)
RioClaroSP
Pmurun
du(FNJV
12976)
81plusmn15(56ndash
103)
152plusmn50(79ndash
247)
9plusmn2(5ndash14)
18plusmn5(10ndash
29)
57557plusmn3226(5168ndash62016)37plusmn04(3-4)
2803
RioClaroSP
Pmurun
du(FNJV
4575)
81plusmn13(54ndash
105)
132plusmn20(97ndash193)
10plusmn2(5ndash16)
23plusmn9(5ndash50)
55755plusmn1493(4875ndash58125)34plusmn07(2ndash5)2843plusmn313(2182ndash3691)
SaoRo
qued
eMinasM
GPmurun
du(FNJV
4576)
118plusmn18(77ndash143)
159plusmn14(129ndash194)
13plusmn2(8ndash18)
27plusmn9(10ndash
54)
54603plusmn766(5250ndash
5625)36plusmn05(2ndash4
)2183plusmn198(1893ndash266
6)
Pocosd
eCaldasMG
Pserran
a(LH673)
98plusmn12(65ndash131)
184plusmn18(131ndash224)
12plusmn2(8ndash18)
16plusmn5(6ndash32)
56556plusmn1202(5168ndash5814)41plusmn03(3ndash5)2183plusmn74(2061ndash
2258)
Brum
adinho
MG
Pserran
a(LH674)
91plusmn14(49ndash
117)236plusmn25(184ndash288)
12plusmn2(6ndash17)
25plusmn8(5ndash4
1)53402plusmn293(5168ndash55125)29plusmn04(2ndash4
)1795plusmn84(1709ndash1877)
Brum
adinho
MG
Pserran
a(LH675)
83plusmn15(49ndash
99)
161plusmn51(81ndash197)
10plusmn2(7ndash16)
16plusmn7(5ndash33)
5857
37plusmn04(3-4)2494plusmn223(2282ndash2727)
SaoJoao
DelRe
iMG
Pserran
a(FNJV
12879)
60plusmn6(47ndash72)
86plusmn8(63ndash101)
8plusmn2(4ndash14)
8plusmn2(4ndash16)
57070plusmn1155(55125ndash5857)39plusmn03(3-4)4119plusmn237(3614ndash4
762)
SaoJoao
DelRe
iMG
Pserran
a(FNJV
12880)
63plusmn13(26ndash
97)
112plusmn20(75ndash166)
5plusmn1(1ndash
9)13plusmn5(4ndash33)
57737plusmn1693(55125ndash60293)38plusmn05(2ndash5)3487plusmn473(2511ndash
5172
)SaoJoao
DelRe
iMG
Psaltica
(13A
-01)
65plusmn9(48ndash86)
120plusmn19(75ndash170)
9plusmn2(5ndash13)
35plusmn14(5ndash55)
47510plusmn1042(460
81ndash49526)25plusmn05(2-3)3839plusmn36(3424ndash4
062)
Chapadad
osGuimaraesMT
Psaltica
(42A
-06)
58plusmn6(46ndash
70)
109plusmn14(90ndash
137)
8plusmn1(4ndash11)
15plusmn7(5ndash30)
49143plusmn353(48234ndash
49526)32plusmn03(3-4)3654plusmn419(2985ndash4
412)
Pontes
eLacerdaM
TPsaltica
(42A
-07)
66plusmn13(48ndash87)
186plusmn23(14
4ndash224)
11plusmn4(4ndash19)
36plusmn5(30ndash
46)
45004plusmn3398(40052ndash49526)22plusmn04(2-3)2393plusmn182(2135ndash283)
Pontes
eLacerdaM
TPsaltica
(LH12)
77plusmn8(63ndash95)
113plusmn18(80ndash
172)
6plusmn1(4ndash9
)21plusmn18(3ndash4
9)50230plusmn1357(48665ndash55125)39plusmn04(3ndash5)3183plusmn328(2299ndash3947)
PortoEstre
laM
TPsaltica
(LH13)
97plusmn6(85ndash106)
127plusmn10(99ndash
158)
5plusmn1(3ndash7)
18plusmn17(2ndash56)
52368plusmn615(50818
ndash52972
)5plusmn01(5ndash6
)2687plusmn147(2308ndash3141)
PortoEstre
laM
TPsaltica
(LH14)
78plusmn5(70ndash
92)
134plusmn17(107ndash210)
17plusmn13(4ndash4
4)6plusmn2(4ndash10)
48062plusmn677(46512
ndash49957)21plusmn03(2-3)2837plusmn253(2062ndash3389)
PortoEstre
laM
TPsaltica
(LH16)
97plusmn10(64ndash
118)
127plusmn18(93ndash162)
10plusmn3(6ndash18)
23plusmn17(3ndash56)
50359plusmn2998(43066ndash
5340
2)45plusmn06(3ndash5)2712plusmn265(2264ndash3352)
PortoEstre
laM
TPsaltica
(LH17)
73plusmn26(33ndash122)
106plusmn24(79ndash
228)
7plusmn1(4ndash8)
19plusmn13(5ndash54)
48837plusmn2099(44789ndash
5168)34plusmn05(3ndash5)3524plusmn776(2113ndash4
838)
PortoEstre
laM
TPsaltica
(LH18)
83plusmn4(75ndash100)
143plusmn17(100ndash212)
5plusmn2(3ndash16)
18plusmn14(3ndash4
7)52483plusmn443(50818
ndash52972
)41plusmn03(4-5)2670plusmn214(1987ndash
3389)
PortoEstre
laM
TPsaltica
(LH709)
86plusmn14(51ndash117
)122plusmn55(58ndash383)
6plusmn1(3ndash10)
11plusmn8(3ndash33)
51139plusmn1169(49967ndash5340
2)44plusmn05(4-5)3067plusmn725(1266ndash4
838)
Uberla
ndiaM
G
6 Advances in Zoology
60∘W 50
∘W 40∘W
0∘
10∘S
20∘S
30∘S
0 400
(km)
PA MA
PICE
4
5
6
MT
32
1
1
7
8
910
11
12
SP
GO
N
Figure 1 Geographical variation in the advertisement calls (oscillograms) of Pseudopaludicola mystacalis from twelve localities in sevenBrazilian states Para (PA) Primavera (1) Ceara (CE) Itapipoca (2) Taıba (3)Maranhao (MA) Balsas (4) Piauı (PI) Brejo do Piauı (5) Goias(GO) Uruacu (6) Mato Grosso (MT) Cuiaba (7) Chapada dos Guimaraes (8) Nossa Senhora do Livramento (9) Pocone (10) Caceres (11)Sao Paulo (SP) Icem (12) Total time of each oscillogram corresponds to 02 s
(Figure 3(c)) and higher loadings corresponded to note rate(385) internote interval (295) and note duration (221) Nodistinct groups were formed along the first function axis ofthe DFA
32 Taxonomic Status of Pseudopaludicola serrana Toledo2010 Advertisement calls of Pseudopaludicola serranarecorded at the type-locality (Brumadinho Minas Gerais)and nearly 120 km southwestwards at Serra do LenheiroMinas Gerais were similar to those of topotypes of P
murundu and distinct from topotypes of P saltica bothin spectral and temporal parameters (Figures 4 and 5)The intraspecific variation in bioacoustic parameters ofP murundu and P serrana presented below is based oncalls from topotypical specimens and on calls recorded inadditional localities listed in Appendix B
Advertisement calls of P serranawere composed of seriesof pulsed notes with nonconcatenated pulses Each note con-sisted of 36plusmn06 (range 2ndash5) pulses Mean note duration was82 plusmn 58ms (26ndash131) emitted on average at intervals of 167 plusmn58ms (63ndash288) Mean duration of each pulse was 9 plusmn 3ms
Advances in Zoology 7
Taiba(CE)
Uruaccedilu(GO)
BBuriti(PI)
C aceres
Livramento (MT)(MT)
(MT)(MT)
(MT) Pocon eCGuimaraes
Cuiab a Itapipoca(CE)
Primavera(PA)
Ic em(SP) Balsas
(MA)
(kH
z)8
7
6
5
4
3
2
1
(s)02 04 06 08 1 12 14 16 18 2 22 24 26 28 3 32 34 36 38
ı
Figure 2 Spectrograms (DFT size = 512 samples) of the advertisement calls of Pseudopaludicola mystacalis from twelve localities (two notesfor each locality) in seven Brazilian states (CE Ceara GO Goias MA Maranhao MT Mato Grosso PA Para PI Piauı SP Sao Paulo)
(2ndash18) Interpulse intervals were 16 plusmn 7ms long (4ndash41) Meanfrequency ranged from 40196 plusmn 453Hz to 70986 plusmn 312Hzand mean dominant frequency was 56251 plusmn 212Hz (5168ndash60293) Advertisement calls of Pmurunduwere composed ofseries of pulsed noteswith nonconcatenated pulses Each noteconsisted of 34 plusmn 06 (range 2ndash5) pulses Mean note durationwas 92 plusmn 18ms (33ndash143) emitted on average at intervals of121 plusmn 30ms (69ndash247) Mean duration of each pulse was 10 plusmn3ms (4ndash18) Interpulse intervals were 24plusmn8ms (5ndash54) Meanfrequency ranged from 36285 plusmn 513Hz to 73301 plusmn 355Hzand mean dominant frequency was 55901 plusmn 176Hz (4875ndash62016Hz)
A discriminant function analysis (DFA)withmorphome-tric data revealed that P serrana and P murundu overlappedalong the first function (DF1) ofDFAwhich explained 98ofthe total variation (Figure 6(a)) While the DFA did not sep-arate P serrana from P murundu both were separated froma third species (Pseudopaludicola saltica) whose individualsalso have long hindlimbs Higher loadings corresponded toeye diameter (121) tarsus length (75) and tibia length (46)DFA from bioacoustic data also separated Pseudopaludicolasaltica from P murundu and P serrana (Figure 6(b))The firstfunction (DF1) of DFA explained 99 of the total variationand higher loadings corresponded to dominant frequency(641) and number of pulses per note (61)
DFAofmorphometricmeasurements using all specimensassigned 100 of the individuals of Pseudopaludicola saltica86 of the individuals of P serrana and only 16 of theindividuals of P murundu to the correct species (Table 5)DFA of bioacoustic variables using all recorded males cor-rectly assigned 89 of the specimens of P saltica 83 of thespecimens of P murundu and 40 of P serrana (Table 5) Incontrast DFA with both morphometric and bioacoustic datausing specimens ofP saltica and amixed sample of specimensattributable to either P murundu or P serrana assigned 100of these latter to a single taxon
The overall similarity in morphology and general struc-ture of the call of P murundu and P serrana evidenced bythe results of DFA with 12 morphometric and six bioacous-tic variables strongly support the rejection of the specificstatus of Pseudopaludicola serrana here considered to be a
junior synonym of Pseudopaludicola murundu Geographi-cal distribution of Pseudopaludicola murundu as presentlyrecognized is not anymore restricted to its type-locality [16]but includes instead twelve distinct localities in southeasternBrazil in the states of Minas Gerais and Sao Paulo (Figure 7)
4 Discussion
41 Geographical Variation in Pseudopaludicola mystacalis(Cope 1887) Among the 18 valid species of Pseudopalu-dicola P mystacalis is currently the one with the mostwidespread distribution range Extent of occurrence in Brazilis nearly two million square kilometers encompassing areasin three different ecoregions along all the ldquodiagonal of openformationsrdquo from South America [23] Caatinga Cerradoand Pantanal It is also found in areas of Chaco in Argentina[24] and Paraguay [25] Although plausible the occurrence inBolivian Chaco was based on material that morphologicallyand bioacoustically would correspond to P ameghini [12 26]Habitats where individuals of this species were found includeldquorestingardquo [10 present study] ldquocampo sujordquo in elevatedplateaus of theCerradoDomain and seasonally floodedfieldsin the Pantanal lowlands [8]
Advertisement calls of Pseudopaludicola mystacalis fromdifferent Brazilian localities are composed of series of noteswith concatenated pulses Maximum variation in dominantfrequency of the calls of all specimens analyzed is 8613Hz(from 44789Hz in Cuiaba Mato Grosso to 53402Hz inBalsas Maranhao Table 3) without any evident latitudinalor longitudinal trend Dominant frequency in the mostdistant known locations (Primavera state of Para and Icemstate of Sao Paulo) varied by 3721 Hz Considering subsetsof populations from Brazilian Northeast (states of CearaMaranhao and Piauı) and from Brazilian Midwest (statesof Mato Grosso and Goias) maximum interpopulationalvariation in dominant frequency is 646Hz and 7752Hzrespectively Maximum intrapopulational variation in dom-inant frequency evaluated for four localities in the lowerportion of the speciesrsquo range (Caceres Cuiaba Nossa Senhorado Livramento and Pocone state ofMatoGrosso) is 5168Hzin Cuiaba (see Table 3 and [8])
8 Advances in Zoology
3
2
1
0
minus1
minus2
210minus1minus2minus3
DF2
(37
)
DF1 (63)
(a)
3
2
1
0
minus1
minus2
minus3
3210minus1minus2minus3minus4
DF2
(15
)
DF1 (85)
(b)
2
1
0
minus1
210minus1minus2
DF1 (79)
DF2
(21
)
Chapada dos Guimaraes-MTCuiab a-MTNS Livramento-MTPorto Estrela-MTC aceres-MTBarra do Garccedilas-MTPocon e-MTUruaccedilu-GO
Alto Alegre-SP
Primavera-PAItapipoca-CETaBalsas-MABrejo do Piauı-PIacute
ıba-CE
Ic em-SP
(c)
Figure 3 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of 101 males (a) 37 females (b)and six bioacoustic variables (c) of Pseudopaludicola mystacalis from 15 different localities in Brazil
Maximum variation in temporal variables (notes perminute and number of pulses) of the calls of all specimensanalyzed is 2136 notesmin and 8 pulsesnote In the mostdistant known locations the difference in the number of notesper minute and in the number of pulses is 1003 notesmin
and 6 pulsesnote respectively Considering subsets of pop-ulations from Brazilian Northeast and Brazilian Midwestmaximum interpopulational variation is 1146 notesmin and1335 notesmin respectively There are 7 pulsesnote in callsfrom populations of both areas Maximum intrapopulational
Advances in Zoology 9
Pseudopaludicola serrana Pseudopaludicola murundu Pseudopaludicola saltica
05 1 15 2 25 3 35 4 45 5
A B C D E F G H I(k
Hz)
8
7
6
5
4
3
2
1
(s)
Figure 4 Spectrograms (DFT size = 512 samples two notes for each locality) of advertisement calls of Pseudopaludicola serrana (AndashC) andP murundu (DndashF) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais-Uberlandia (G) state of MatoGrosso-Chapada dos Guimaraes (type-locality H) and Porto Estrela (I)
Note Pulses
(a) (b)
(c) (d)
(e) (f)
(g) (h)
Figure 5 Oscillograms of advertisement calls of Pseudopaludicola serrana (a)-(b) and P murundu (c)ndash(e) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais Uberlandia (f) state of Mato Grosso Chapada dos Guimaraes (type-locality (g))and Porto Estrela (h) Total time of each oscillogram corresponds to 05 s
10 Advances in Zoology
4
2
0
minus2
minus4
6420minus2minus4
DF2
(2
)
DF1 (98)
(a)
4
2
0
minus2
minus4
6420minus2minus4
DF2
(1
)
DF1 (99)
(b)
Figure 6 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of males (a) and six bioacousticvariables (b) of Pseudopaludicola murundu (open circles) P saltica (triangles) and P serrana (closed circles)
Elevation (m)
0
(km)
minus155ndash350351ndash700701ndash1050
1050ndash14001401ndash1750
300
N
1
2
3
4
5
6 78
91011
12
13
Figure 7 Geographical distribution of Pseudopaludicola murundu(circles) and P saltica (triangles) in southeastern Brazil state of SaoPaulomdashRioClaro (type locality (1)) andCampinas (2) state ofMinasGeraismdashPocos de Caldas (3) Alpinopolis (4) (see [17]) Sao Roquede Minas (5) Sao Joao Del Rei (6) Mariana (7) Ouro Branco (8)Itabirito (9) Brumadinho (10) Lavras Novas (11) Botumirim (12)and Uberlandia (13)
variation in the number of notes per minute and in thenumber of pulses in four localities from the state of MatoGrosso is 81 notesmin in Cuiaba and 5 pulsesnote in Cuiabaand Nossa Senhora do Livramento (see Table 3 and [8])Mean note duration does not differ significantly in all theexamined calls (Table 3 119865 = 49 df = 2 119875 = 003)
Table 5 Summary of the number of male specimens correctlyclassified as Pseudopaludicolamurundu P saltica or P serrana usingdiscriminant function analysis of 12 morphometric measurementsand seven bioacoustic variables
Morphometric measurementsTrue group
P murundu P saltica P serranaP murundu 1 0 5P saltica 0 39 0P serrana 3 0 19Total number 6 39 22 16 100 86
Bioacoustic variablesTrue group
P murundu P saltica P serranaP murundu 5 0 1P saltica 0 8 1P serrana 3 0 2Total number 6 9 5 83 889 40
Acoustic analysis of geographical variation in specieswith an extent of occurrence of the magnitude seen inP mystacalis sometimes reveals cryptic taxa being treatedunder a single name However this was not the case in Pmystacalis a taxon that remained erroneously characterizedand poorly recognized in the literature until recently [8] Ourresults reveal a relatively small variation in morphologicaland acoustical traits of P mystacalis and allow confirming thepresence of the species in a wide geographical area along theBrazilian open ecosystems
Advances in Zoology 11
Table 6 Ratios of selected measurements (in mm) of males of Pseudopaludicola murundu P salticaand P serrana Values are presented asmean plusmn standard deviation119873 = number of specimens analyzed
HLSVL HWSVL HLHW HALSVL FLSVL THLSVL TLSVLP serrana (119873 = 21) 040 plusmn 003 036 plusmn 002 110 plusmn 006 027 plusmn 002 061 plusmn 004 056 plusmn 003 070 plusmn 003
P murundu (119873 = 5) 039 plusmn 004 035 plusmn 003 111 plusmn 009 027 plusmn 001 066 plusmn 002 056 plusmn 002 070 plusmn 003
P saltica (119873 = 44) 041 plusmn 004 038 plusmn 003 109 plusmn 011 026 plusmn 003 068 plusmn 006 055 plusmn 005 073 plusmn 005
HAL hand length HL head length HW head width FL foot length SVL snout-vent length THL thigh length TL tibia length
42 Taxonomic Status of Pseudopaludicola serrana Toledo2010 When describing P serrana Toledo [15] used asmorphological characteristics separating the three speciesbelonging to the P saltica group the aspect (relative size andcoloration) of nuptial pads in the external part of finger I andaspect of the vocal sac Such characteristics allow differingP serrana and P murundu from P saltica but do not allowdiffering P serrana from P murundu [15] Previously Haddadand Cardoso [17] had called attention to the fact that nuptialpads were more developed in specimens of P saltica from thetype-locality (Chapada do Guimaraes Mato Grosso) than inspecimens collected and recorded in localities in the statesof Minas Gerais and Sao Paulo In the same article Haddadand Cardoso [17] also presented a spectrogram of the callof a specimen from Campinas Sao Paulo Based on suchreported morphological evidence and acoustic parameterswe here argue that specimens from Minas Gerais and SaoPaulo attributed to P saltica in Haddad and Cardoso [17] infact correspond to P murundu
The only external morphological characteristic used byToledo [15] to differ P serrana from P murunduwas a shorterhead lengthheadwidth ratio (HLHW= 097plusmn006 in the fiveindividuals ofP serrana evaluated 111plusmn007 in 11 individualsof P murundu) After having analyzed a higher number ofspecimens attributed to P serrana (119873 = 21) we found thatHLHW (110 plusmn 006 see Table 6) in this sample does notdiffer from the values presented in the original descriptionand confirmed herein for P murundu
The description of P serrana was also based on physicalcharacteristics of its advertisement calls [15] However theoriginal dataset is relatively low 12 notes of a single maleof P saltica 14 notes of 2 males of P murundu and 15notes of 3 males of P serrana were analyzed and comparedOnly one out of four acoustic variables (pulse duration) wasconsidered diagnostic for the new species Toledo [15] alsoshowed that dominant frequency range of P serrana wascompletely nested within the dominant frequency range of Pmurundu However when later proposing the synonymiza-tion of Pseudopaludicola riopiedadensis Mercadal de Bar-rio and Barrio 1994 to Pseudopaludicola ternetzi Miranda-Ribeiro 1937 Cardozo and Toledo [5] based their decision onldquoseveral important overlapsrdquo including dominant frequencyranges between the two species Indeed our data showedthat dominant frequency contributed to higher loadingsto separate species in the P saltica group Nonoverlappingdominant frequencies would therefore be expected betweenrelated but distinct species of Pseudopaludicola
Bioacoustic data have proven to be useful for uncoveringmorphologically cryptic species in the genus Pseudopaludi-cola [4ndash9 15 16] Advertisement calls of species in this genusmight be divided into three distinct groups according to typeof notes nonpulsed notes notes with concatenated pulsesand noteswith nonconcatenated pulses [7] Each groupmightbe diagnosed by temporal (pulses per note note and pulseduration internotes and interpulses intervals note rate andpulse rate) and spectral variables (dominant frequency andharmonics) which in combination allow characterizing allthe species for which calls were already analyzed except forP serrana and P murundu As evidenced by the recent syn-onymization of Pseudopaludicola riopiedadensis to P ternetzi[15] and reinforced herein by the proposed synonymizationof P serrana to P murundu morphologically similar speciesof Pseudopaludicola presenting the same type of note and anoverlap in their spectral acoustic variables are expected torepresent the same taxon Therefore no arguments remainto consider P serrana as a distinct species from P murunduand the former must be considered as a junior synonym of Pmurundu
5 Conclusions
We here report on the variation in morphometric charactersand variation in bioacoustic variables of the advertisementcalls in fifteen Brazilian populations of Pseudopaludicolamys-tacalis Although limited our sample evidenced no statisticaldifferences in any of the evaluated attributes and allowed usto confirm that this species is widely distributed in BrazilMorphometric and bioacoustic data did not differ also inpopulations currently attributed to Pseudopaludicola serranaand Pseudopaludicola murundu and the former taxon ishere considered as a junior synonym of P murundu Thedata in the present work aims at contributing to a betterunderstanding of the diversity and distribution patterns inthe genus Pseudopaludicola
Appendices
A Voucher Specimens Examined
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality 22∘1910158405210158401015840S 47∘4210158405610158401015840W)-F UFMT 18454MUFMT 18395-6 UFMT 18455-7
Pseudopaludicola mystacalis Brazil Para Primavera(00∘5710158402210158401015840S 47∘0710158401210158401015840W)-M UFMT 11651 UFMT 11827
12 Advances in Zoology
UFMT 11833 UFMT 11836 UFMT 11839 Goias Uruacu(14∘3110158403510158401015840S 49∘0710158405410158401015840W)-F UFMT 18397-400 UFMT18458-9 M UFMT 18401-15 UFMT 18458-64 Mato GrossoBarra do Garcas (15∘3110158405710158401015840S 52∘1410158401010158401015840W)-M UFMT11097 UFMT 11307 UFMT 11319 UFMT 11324 Caceres(16∘1710158405910158401015840S 58∘0910158400910158401015840W)-F UFMT 5906 UFMT 5950UFMT 5955 UFMT 5962 UFMT 9152 UFMT 10445UFMT 10448 UFMT 13669 M UFMT 10451-2 UFMT10455 UFMT 10458 UFMT 10466 UFMT 10495 UFMT10506 UFMT 10508 UFMT 13670 Chapada dos Guimaraes(type-locality 14∘5010158403410158401015840S 55∘2310158401010158401015840W)-F UFMT 8109 MUFMT 487 UFMT 817 UFMT 820 UFMT 12890 Cuiaba(15∘3910158403310158401015840S 55∘5610158403010158401015840W)-M UFMT 15980 UFMT 2426UFMT 2430 UFMT 2432 UFMT 2434-7 UFMT 2439UFMT 7399 UFMT 7653 UFMT 8177-8 UFMT 8180UFMT 8182 UFMT 8184-5 UFMT 13671 Nossa Senhorado Livramento (16∘2110158405810158401015840S 56∘1810158403310158401015840W)-F UFMT 18465UFMT 352 UFMT 6436 UFMT 6466-7 UFMT 6488UFMT 6511 M UFMT 4343 UFMT 6487 UFMT 6491UFMT6498UFMT6515Pocone (16∘3010158405810158401015840S 56∘4410158405310158401015840W)-M UFMT 348-50 UFMT 889 UFMT 4316 UFMT 4318UFMT 4321 UFMT 13672 and Porto Estrela (15∘3510158400510158401015840S57∘1310158402010158401015840W)-F UFMT 18466-7 UFMT 138 UFMT 13482M UFMT 18468-9 UFMT 402 UFMT 2200 UFMT 11346Sao Paulo Icem (20∘2010158403110158401015840S 49∘1110158404210158401015840W)-F UFMT 18421UFMT 18470-2 M UFMT 18422-3 UFMT 18473 and AltoAlegre (21∘3310158402010158401015840S 50∘1310158402210158401015840W)-F UFMT 18474-5 UFMT18479 MUFMT 18476-8 UFMT 18480-6
Pseudopaludicola saltica Brazil Mato Grosso Chapadados Guimaraes (type-locality 15∘2310158400910158401015840S 55∘5010158402410158401015840W)-MUFMT 482 UFMT 819 UFMT 821 UFMT 823 UFMT 1433-5 UFMT 1437-41 UFMT 2873 UFMT 2877 UFMT 2880-1F UFMT 1442 Cuiaba M UFMT 270 UFMT 473 UFMT476 UFMT 13657-68 F UFMT 13655-6) Nova Lacerda (MUFMT 13499-501) Porto Estrela Estacao Ecologica da Serradas Araras (M UFMT 561) and Vila Bela da SantıssimaTrindade (M UFMT 4082 UFMT 4112 UFMT 4123 UFMT4147 UFMT4153 UFMT4157 UFMT4172)MatoGrosso doSul Sonora (M UFMT 1147 UFMT 1195)
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho (type-locality 20∘0610158403210158401015840S 43∘5810158405310158401015840W)-F MCNAM 3675 MUFMT 18424 UFMT 18451 MCNAM 3677-8 MCNAM3680 Itabirito (20∘1310158402910158401015840S 43∘4810158404910158401015840W)-F MCNAM14620-1 M MCNAM 14625 Lavras Novas (20∘2810158405710158401015840S43∘3010158405210158401015840W)-F MCNAM 3694 M MCNAM 3695MCNAM 3690 Mariana (20∘0910158401210158401015840S 43∘3010158400210158401015840W)-FMCNAM 6465 M MCNAM 6457 MCNAM 6461-2 OuroBranco (20∘3010158401610158401015840S 43∘4210158400410158401015840W)-M MCNAM 6559 SaoJoao Del Rei (21∘0810158402510158401015840S 44∘1710158403110158401015840W)-M UFMT 18425-6UFMT 18452-3 and Botumirim (16∘4410158401310158401015840S 42∘3410158402910158401015840W)-FMCNAM 6713 M MCNAM 6832 MCNAM 6834 MCNAM6636 MCNAM 6642-3
B Analyzed Sound Files
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality) LH 676 no voucher specimen LH 677 call
fromUFMT 18455 LH 678 call fromUFMT 18395 and FNJV12976 no voucher specimen Minas Gerais Sao Roque deMinas (20∘1310158402010158401015840S 46∘2710158402410158401015840W) FNJV 4575 no voucherspecimen and Pocos de Caldas (21∘5510158400410158401015840S 46∘3410158400210158401015840W)FNJV 4576 no voucher specimen
Pseudopaludicola mystacalis Brazil Ceara Itapipoca(03∘2410158405810158401015840S 39∘4110158403110158401015840W) LH 655 no voucher specimenTaiba (03∘2510158404410158401015840S 38∘5710158404310158401015840W) LH 658 no voucher spec-imen Goias Uruacu LH 639 call from UFMT 18410) MatoGrosso Chapada dos Guimaraes (type-locality) LH 13A-05no voucher specimen) Caceres LH 47A-04 call fromUFMT10451 Cuiaba LH 14A-01 call from UFMT 2426 LH 14A-02 call from UFMT 2424 Pocone LH 01A-01 call fromUFMT 4321 and Nossa Senhora do Livramento LH 04A-10 call from UFMT 4330 Maranhao Balsa (07∘2810158404910158401015840S46∘0310158401910158401015840W) LH 284 no voucher specimen Piauı Brejo doPiauı (08∘1110158405010158401015840S 42∘4910158405910158401015840W) LH 184 call from UFMT11202 Para Primavera LH 352 call from UFMT 11836 SaoPaulo Icem LH 701 call from UFMT 18423
Pseudopaludicola saltica BrazilMatoGrossoCuiaba LH13A-01 call fromUFMT 8187Nova Lacerda LH 42A-06 callfrom UFMT 13499 LH 42A-07 call from UFMT 13500 andPorto Estrela LH 12 no voucher specimen LH 13 call fromUFMT 13678 LH 14 call fromUFMT 16423 LH 16 call fromUFMT 16417 LH 17 call from UFMT 16414 and LH 18 callfrom UFMT 16385 Minas Gerais Uberlandia (18∘5810158403010158401015840S48∘1710158402610158401015840W) LH 709 no voucher specimen
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho LH 673call from UFMT 18451 LH 674 no voucher specimen andSao Joao Del Rei LH 675 call from UFMT 18426 and FNJV12879-80 no voucher specimen
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Special thanks go to Felipe Franco Curcio Diva MariaBorges-Nojosa and Luciana Barreto Nascimento for allow-ing access to the material under their care at ldquoColecaoZoologica de Vertebrados da Universidade Federal de MatoGrossordquo (UFMT) ldquoColecao Herpetologica da UniversidadeFederal do Cearardquo (UFC) and ldquoMuseu de Ciencias Naturaisrdquo(MCNAM Belo Horizonte Minas Gerais) respectively toAdao J Cardoso (in memoriam) and Luis F Toledo for therecordings and for allowing access respectively to bioa-coustic samples deposited at ldquoFonoteca Neotropical JacquesVielliardrdquo (FNJV) to the CNPq project ldquoRede de pesquisa emanfıbios e repteis de ecossistemas nao florestais brasileirosrdquo(Process no 5633522010-8) for logistical support to VivianUhlig (RANICMBio) for estimates of extent of occurrenceAndre Pansonato thanks ldquoCoordenacao de Aperfeicoamentode Pessoal de Nivel Superiorrdquo (CAPES) for a PhD scholar-ship and Christine Strussmann thanks CNPq for a researchfellowship (Process no 3095412012-3)
Advances in Zoology 13
References
[1] K D Wells The Ecology amp Behavior of Amphibians TheUniversity of Chicago Chicago Ill USA 2007
[2] M Vences M Gehara J Kohler and F Glaw ldquoDescription of anewMalagasy treefrog (Boophis) occurring syntopically with itssister species and a plea for studies on non-allopatric speciationin tropical amphibiansrdquo Amphibia Reptilia vol 33 no 3-4 pp503ndash520 2012
[3] I De La Riva R Marquez and J Bosch ldquoDescription ofthe advertisement calls of some South American Hylidae(Amphibia Anura) taxonomic and methodological conse-quencesrdquo Bonner Zoologische Beitrage vol 47 pp 175ndash185 1997
[4] F S de Andrade and T R de Carvalho ldquoA new species of Pseu-dopaludicola Miranda-Ribeiro (Leiuperinae LeptodactylidaeAnura) from the Cerrado of southeastern Brazilrdquo Zootaxa vol3608 no 5 pp 389ndash397 2013
[5] D Cardozo and L F Toledo ldquoTaxonomic status of Pseudopalu-dicola riopiedadensis Mercadal de Barrio and Barrio 1994(Anura Leptodactylidae Leiuperinae)rdquo Zootaxa vol 3734 pp571ndash582 2013
[6] T R de Carvalho ldquoA new species of PseudopaludicolaMiranda-Ribeiro (Leiuperinae Leptodactylidae Anura) from the Cer-rado of southeastern Brazil with a distinctive advertisement callpatternrdquo Zootaxa no 3328 pp 47ndash54 2012
[7] F M Magalhaes D Loebmann M N C Kokubum C F BHaddad and A A Garda ldquoA new species of Pseudopaludi-cola (Anura Leptodactylidae Leiuperinae) from NortheasternBrazilrdquo Herpetologica vol 70 pp 77ndash88 2014
[8] A Pansonato C Strussmann J R Mudrek and I A Mar-tins ldquoMorphometric and bioacoustic data on three species ofPseudopaludicola Miranda-Ribeiro 1926 (Anura Leptodactyl-idae Leiuperinae) described from Chapada dos GuimaraesMato Grosso Brazil with the revalidation of Pseudopaludicolaameghini (Cope 1887)rdquo Zootaxa vol 3620 no 1 pp 147ndash1622013
[9] I J Roberto D Cardozo and R W Avila ldquoA new speciesof Pseudopaludicola (Anura Leiuperidae) from Western PiauıState Northeast Brazilrdquo Zootaxa vol 3636 no 2 pp 348ndash3602013
[10] S B Barreto M S Tinoco D Couto-Ferreira and H CBrowne-Ribeiro ldquoDistribuicao de Pseudopaludicola aff falcipes(Anura Leiuperidae) na restinga do litoral norte da BahiaBrasilrdquoRevista Latino-Americana de Conservacao vol 2 pp 27ndash36 2012
[11] E R Favero A C P Veiga-Menoncello D C Rossa-Feres et alldquoIntrageneric karyotypic variation in Pseudopaludicola (AnuraLeiuperidae) and its taxonomic relatednessrdquo Zoological Studiesvol 50 no 6 pp 826ndash836 2011
[12] M Jansen R Bloch A Schulze andM Pfenninger ldquoIntegrativeinventory of Boliviarsquos lowland anurans reveals hidden diversityrdquoZoologica Scripta vol 40 no 6 pp 567ndash583 2011
[13] C P D Prado M Uetanabaro and C F B Haddad ldquoBreed-ing activity patterns reproductive modes and habitat use byanurans (Amphibia) in a seasonal environment in the PantanalBrazilrdquo Amphibia Reptilia vol 26 no 2 pp 211ndash221 2005
[14] R A Silva I A Martins and D C Rossa-Feres ldquoBioacustica esıtio de vocalizacao em taxocenoses de anfıbios de area abertano Noroeste Paulistardquo Biota Neotropica vol 8 pp 123ndash1342008
[15] L F Toledo ldquoDescription of a new species of PseudopaludicolaMiranda-Ribeiro 1926 from the state of Sao Paulo SoutheasternBrazil (Anura Leiuperidae)rdquoZootaxa no 2681 pp 47ndash56 2010
[16] L F Toledo S Siqueira T CDuarte A C P Veiga-MenoncelloS M Recco-Pimentel and C F B Haddad ldquoDescription of anew species of Pseudopaludicola Miranda-Ribeiro 1926 fromthe state of Sao Paulo Southeastern Brazil (Anura Leiuperi-dae)rdquo Zootaxa no 2496 pp 38ndash48 2010
[17] C F B Haddad and A J Cardoso ldquoTaxonomia de tres especiesde Pseudopaludicola (Anura Leptodactylidae)rdquo Papeis Avulsosde Zoologia vol 36 pp 287ndash300 1987
[18] T C Duarte A C P Veiga-Menoncello J F R Lima et alldquoChromosome analysis in Pseudopaludicola (Anura Leiuperi-dae) with description of sex chromosomes XXXY in P salticardquoHereditas vol 147 no 2 pp 43ndash52 2010
[19] A C P Veiga-Menoncello L B Lourenco C Strussmannet al ldquoA phylogenetic analysis of Pseudopaludicola (Anura)providing evidence of progressive chromosome reductionrdquoZoologica Scripta vol 43 no 3 pp 261ndash272 2014
[20] W R Heyer A S Rand C A G Cruz O L Peixoto and CE Nelson ldquoFrogs of Boraceiardquo Arquivos de Zoologia vol 31 pp231ndash410 1990
[21] W E Duellman The Hylid Frogs of Middle America vol 1 ofMonograph of the Museum of Natural History of University ofKansas 1970
[22] R Development Core Team The R Project for Statistical Com-puting Vienna Austria 2013 httpwwwr-projectorg
[23] P E Vanzolini ldquoEcological and geographical distribution oflizards in Pernambuco Northeastern Brasil (Sauria)rdquo PapeisAvulsos de Zoologia vol 18 no 4 pp 61ndash90 1974
[24] J M Cei ldquoAmphibians of Argentinardquo Monitore ZoologicoItaliano Nuova Serie Monografia vol 2 pp 1ndash609 1980
[25] F Brusquetti and E O Lavilla ldquoLista comentada de los anfibiosde ParaguayrdquoCuadernos deHerpetologıa vol 20 no 2 pp 3ndash792006
[26] I De La Riva J Kohler S Lotters and S Reichle ldquoTenyears of research on Bolivian amphibians updated checklistdistribution taxonomic problems literature and iconographyrdquoRevista Espanola Herpetologica vol 14 pp 19ndash164 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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PeptidesInternational Journal of
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International Journal of
Volume 2014
Zoology
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Molecular Biology International
GenomicsInternational Journal of
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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
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BioinformaticsAdvances in
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Signal TransductionJournal of
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International Journal of
Microbiology
Advances in Zoology 5
Table4
Measurementsof
bioacoustic
varia
bles
oftheadvertise
mentc
allsof
specim
enso
fPseud
opalud
icola
murun
duPsalticaandPserranaVa
lues
arepresentedas
meanplusmnsta
ndard
deviation(m
inim
umndashm
axim
um)
Species
(vou
cher
record)
Noted
uration(m
s)Internoteinterval(ms)
Pulse
duratio
n(m
s)Interpulsesinterval(ms)
Dom
inantfrequ
ency
(Hz)
Pulse
sno
teNotesm
inMun
icipality
state
Pmurun
du(LH676)
80plusmn12(58ndash105)
100plusmn15(69ndash
141)
8plusmn2(4ndash12)
26plusmn7(7ndash4
0)56007plusmn2043(5168ndash5857)33plusmn07(2ndash5)3489plusmn219(3145ndash3704)
RioClaroSP
Pmurun
du(LH677)
94plusmn11(49ndash
114)
98plusmn16(70ndash
140)
13plusmn2(9ndash17)
23plusmn9(6ndash39)
55799plusmn1502(52541ndash5857)29plusmn02(2-3)3172plusmn176(2956ndash3419)
RioClaroSP
Pmurun
du(LH678)
89plusmn13(33ndash104)
107plusmn12(89ndash
137)
9plusmn2(5ndash17)
20plusmn8(8ndash4
6)57259plusmn1297(53402ndash59001)37plusmn05(2ndash4
)3087plusmn139(2926ndash3264)
RioClaroSP
Pmurun
du(FNJV
12976)
81plusmn15(56ndash
103)
152plusmn50(79ndash
247)
9plusmn2(5ndash14)
18plusmn5(10ndash
29)
57557plusmn3226(5168ndash62016)37plusmn04(3-4)
2803
RioClaroSP
Pmurun
du(FNJV
4575)
81plusmn13(54ndash
105)
132plusmn20(97ndash193)
10plusmn2(5ndash16)
23plusmn9(5ndash50)
55755plusmn1493(4875ndash58125)34plusmn07(2ndash5)2843plusmn313(2182ndash3691)
SaoRo
qued
eMinasM
GPmurun
du(FNJV
4576)
118plusmn18(77ndash143)
159plusmn14(129ndash194)
13plusmn2(8ndash18)
27plusmn9(10ndash
54)
54603plusmn766(5250ndash
5625)36plusmn05(2ndash4
)2183plusmn198(1893ndash266
6)
Pocosd
eCaldasMG
Pserran
a(LH673)
98plusmn12(65ndash131)
184plusmn18(131ndash224)
12plusmn2(8ndash18)
16plusmn5(6ndash32)
56556plusmn1202(5168ndash5814)41plusmn03(3ndash5)2183plusmn74(2061ndash
2258)
Brum
adinho
MG
Pserran
a(LH674)
91plusmn14(49ndash
117)236plusmn25(184ndash288)
12plusmn2(6ndash17)
25plusmn8(5ndash4
1)53402plusmn293(5168ndash55125)29plusmn04(2ndash4
)1795plusmn84(1709ndash1877)
Brum
adinho
MG
Pserran
a(LH675)
83plusmn15(49ndash
99)
161plusmn51(81ndash197)
10plusmn2(7ndash16)
16plusmn7(5ndash33)
5857
37plusmn04(3-4)2494plusmn223(2282ndash2727)
SaoJoao
DelRe
iMG
Pserran
a(FNJV
12879)
60plusmn6(47ndash72)
86plusmn8(63ndash101)
8plusmn2(4ndash14)
8plusmn2(4ndash16)
57070plusmn1155(55125ndash5857)39plusmn03(3-4)4119plusmn237(3614ndash4
762)
SaoJoao
DelRe
iMG
Pserran
a(FNJV
12880)
63plusmn13(26ndash
97)
112plusmn20(75ndash166)
5plusmn1(1ndash
9)13plusmn5(4ndash33)
57737plusmn1693(55125ndash60293)38plusmn05(2ndash5)3487plusmn473(2511ndash
5172
)SaoJoao
DelRe
iMG
Psaltica
(13A
-01)
65plusmn9(48ndash86)
120plusmn19(75ndash170)
9plusmn2(5ndash13)
35plusmn14(5ndash55)
47510plusmn1042(460
81ndash49526)25plusmn05(2-3)3839plusmn36(3424ndash4
062)
Chapadad
osGuimaraesMT
Psaltica
(42A
-06)
58plusmn6(46ndash
70)
109plusmn14(90ndash
137)
8plusmn1(4ndash11)
15plusmn7(5ndash30)
49143plusmn353(48234ndash
49526)32plusmn03(3-4)3654plusmn419(2985ndash4
412)
Pontes
eLacerdaM
TPsaltica
(42A
-07)
66plusmn13(48ndash87)
186plusmn23(14
4ndash224)
11plusmn4(4ndash19)
36plusmn5(30ndash
46)
45004plusmn3398(40052ndash49526)22plusmn04(2-3)2393plusmn182(2135ndash283)
Pontes
eLacerdaM
TPsaltica
(LH12)
77plusmn8(63ndash95)
113plusmn18(80ndash
172)
6plusmn1(4ndash9
)21plusmn18(3ndash4
9)50230plusmn1357(48665ndash55125)39plusmn04(3ndash5)3183plusmn328(2299ndash3947)
PortoEstre
laM
TPsaltica
(LH13)
97plusmn6(85ndash106)
127plusmn10(99ndash
158)
5plusmn1(3ndash7)
18plusmn17(2ndash56)
52368plusmn615(50818
ndash52972
)5plusmn01(5ndash6
)2687plusmn147(2308ndash3141)
PortoEstre
laM
TPsaltica
(LH14)
78plusmn5(70ndash
92)
134plusmn17(107ndash210)
17plusmn13(4ndash4
4)6plusmn2(4ndash10)
48062plusmn677(46512
ndash49957)21plusmn03(2-3)2837plusmn253(2062ndash3389)
PortoEstre
laM
TPsaltica
(LH16)
97plusmn10(64ndash
118)
127plusmn18(93ndash162)
10plusmn3(6ndash18)
23plusmn17(3ndash56)
50359plusmn2998(43066ndash
5340
2)45plusmn06(3ndash5)2712plusmn265(2264ndash3352)
PortoEstre
laM
TPsaltica
(LH17)
73plusmn26(33ndash122)
106plusmn24(79ndash
228)
7plusmn1(4ndash8)
19plusmn13(5ndash54)
48837plusmn2099(44789ndash
5168)34plusmn05(3ndash5)3524plusmn776(2113ndash4
838)
PortoEstre
laM
TPsaltica
(LH18)
83plusmn4(75ndash100)
143plusmn17(100ndash212)
5plusmn2(3ndash16)
18plusmn14(3ndash4
7)52483plusmn443(50818
ndash52972
)41plusmn03(4-5)2670plusmn214(1987ndash
3389)
PortoEstre
laM
TPsaltica
(LH709)
86plusmn14(51ndash117
)122plusmn55(58ndash383)
6plusmn1(3ndash10)
11plusmn8(3ndash33)
51139plusmn1169(49967ndash5340
2)44plusmn05(4-5)3067plusmn725(1266ndash4
838)
Uberla
ndiaM
G
6 Advances in Zoology
60∘W 50
∘W 40∘W
0∘
10∘S
20∘S
30∘S
0 400
(km)
PA MA
PICE
4
5
6
MT
32
1
1
7
8
910
11
12
SP
GO
N
Figure 1 Geographical variation in the advertisement calls (oscillograms) of Pseudopaludicola mystacalis from twelve localities in sevenBrazilian states Para (PA) Primavera (1) Ceara (CE) Itapipoca (2) Taıba (3)Maranhao (MA) Balsas (4) Piauı (PI) Brejo do Piauı (5) Goias(GO) Uruacu (6) Mato Grosso (MT) Cuiaba (7) Chapada dos Guimaraes (8) Nossa Senhora do Livramento (9) Pocone (10) Caceres (11)Sao Paulo (SP) Icem (12) Total time of each oscillogram corresponds to 02 s
(Figure 3(c)) and higher loadings corresponded to note rate(385) internote interval (295) and note duration (221) Nodistinct groups were formed along the first function axis ofthe DFA
32 Taxonomic Status of Pseudopaludicola serrana Toledo2010 Advertisement calls of Pseudopaludicola serranarecorded at the type-locality (Brumadinho Minas Gerais)and nearly 120 km southwestwards at Serra do LenheiroMinas Gerais were similar to those of topotypes of P
murundu and distinct from topotypes of P saltica bothin spectral and temporal parameters (Figures 4 and 5)The intraspecific variation in bioacoustic parameters ofP murundu and P serrana presented below is based oncalls from topotypical specimens and on calls recorded inadditional localities listed in Appendix B
Advertisement calls of P serranawere composed of seriesof pulsed notes with nonconcatenated pulses Each note con-sisted of 36plusmn06 (range 2ndash5) pulses Mean note duration was82 plusmn 58ms (26ndash131) emitted on average at intervals of 167 plusmn58ms (63ndash288) Mean duration of each pulse was 9 plusmn 3ms
Advances in Zoology 7
Taiba(CE)
Uruaccedilu(GO)
BBuriti(PI)
C aceres
Livramento (MT)(MT)
(MT)(MT)
(MT) Pocon eCGuimaraes
Cuiab a Itapipoca(CE)
Primavera(PA)
Ic em(SP) Balsas
(MA)
(kH
z)8
7
6
5
4
3
2
1
(s)02 04 06 08 1 12 14 16 18 2 22 24 26 28 3 32 34 36 38
ı
Figure 2 Spectrograms (DFT size = 512 samples) of the advertisement calls of Pseudopaludicola mystacalis from twelve localities (two notesfor each locality) in seven Brazilian states (CE Ceara GO Goias MA Maranhao MT Mato Grosso PA Para PI Piauı SP Sao Paulo)
(2ndash18) Interpulse intervals were 16 plusmn 7ms long (4ndash41) Meanfrequency ranged from 40196 plusmn 453Hz to 70986 plusmn 312Hzand mean dominant frequency was 56251 plusmn 212Hz (5168ndash60293) Advertisement calls of Pmurunduwere composed ofseries of pulsed noteswith nonconcatenated pulses Each noteconsisted of 34 plusmn 06 (range 2ndash5) pulses Mean note durationwas 92 plusmn 18ms (33ndash143) emitted on average at intervals of121 plusmn 30ms (69ndash247) Mean duration of each pulse was 10 plusmn3ms (4ndash18) Interpulse intervals were 24plusmn8ms (5ndash54) Meanfrequency ranged from 36285 plusmn 513Hz to 73301 plusmn 355Hzand mean dominant frequency was 55901 plusmn 176Hz (4875ndash62016Hz)
A discriminant function analysis (DFA)withmorphome-tric data revealed that P serrana and P murundu overlappedalong the first function (DF1) ofDFAwhich explained 98ofthe total variation (Figure 6(a)) While the DFA did not sep-arate P serrana from P murundu both were separated froma third species (Pseudopaludicola saltica) whose individualsalso have long hindlimbs Higher loadings corresponded toeye diameter (121) tarsus length (75) and tibia length (46)DFA from bioacoustic data also separated Pseudopaludicolasaltica from P murundu and P serrana (Figure 6(b))The firstfunction (DF1) of DFA explained 99 of the total variationand higher loadings corresponded to dominant frequency(641) and number of pulses per note (61)
DFAofmorphometricmeasurements using all specimensassigned 100 of the individuals of Pseudopaludicola saltica86 of the individuals of P serrana and only 16 of theindividuals of P murundu to the correct species (Table 5)DFA of bioacoustic variables using all recorded males cor-rectly assigned 89 of the specimens of P saltica 83 of thespecimens of P murundu and 40 of P serrana (Table 5) Incontrast DFA with both morphometric and bioacoustic datausing specimens ofP saltica and amixed sample of specimensattributable to either P murundu or P serrana assigned 100of these latter to a single taxon
The overall similarity in morphology and general struc-ture of the call of P murundu and P serrana evidenced bythe results of DFA with 12 morphometric and six bioacous-tic variables strongly support the rejection of the specificstatus of Pseudopaludicola serrana here considered to be a
junior synonym of Pseudopaludicola murundu Geographi-cal distribution of Pseudopaludicola murundu as presentlyrecognized is not anymore restricted to its type-locality [16]but includes instead twelve distinct localities in southeasternBrazil in the states of Minas Gerais and Sao Paulo (Figure 7)
4 Discussion
41 Geographical Variation in Pseudopaludicola mystacalis(Cope 1887) Among the 18 valid species of Pseudopalu-dicola P mystacalis is currently the one with the mostwidespread distribution range Extent of occurrence in Brazilis nearly two million square kilometers encompassing areasin three different ecoregions along all the ldquodiagonal of openformationsrdquo from South America [23] Caatinga Cerradoand Pantanal It is also found in areas of Chaco in Argentina[24] and Paraguay [25] Although plausible the occurrence inBolivian Chaco was based on material that morphologicallyand bioacoustically would correspond to P ameghini [12 26]Habitats where individuals of this species were found includeldquorestingardquo [10 present study] ldquocampo sujordquo in elevatedplateaus of theCerradoDomain and seasonally floodedfieldsin the Pantanal lowlands [8]
Advertisement calls of Pseudopaludicola mystacalis fromdifferent Brazilian localities are composed of series of noteswith concatenated pulses Maximum variation in dominantfrequency of the calls of all specimens analyzed is 8613Hz(from 44789Hz in Cuiaba Mato Grosso to 53402Hz inBalsas Maranhao Table 3) without any evident latitudinalor longitudinal trend Dominant frequency in the mostdistant known locations (Primavera state of Para and Icemstate of Sao Paulo) varied by 3721 Hz Considering subsetsof populations from Brazilian Northeast (states of CearaMaranhao and Piauı) and from Brazilian Midwest (statesof Mato Grosso and Goias) maximum interpopulationalvariation in dominant frequency is 646Hz and 7752Hzrespectively Maximum intrapopulational variation in dom-inant frequency evaluated for four localities in the lowerportion of the speciesrsquo range (Caceres Cuiaba Nossa Senhorado Livramento and Pocone state ofMatoGrosso) is 5168Hzin Cuiaba (see Table 3 and [8])
8 Advances in Zoology
3
2
1
0
minus1
minus2
210minus1minus2minus3
DF2
(37
)
DF1 (63)
(a)
3
2
1
0
minus1
minus2
minus3
3210minus1minus2minus3minus4
DF2
(15
)
DF1 (85)
(b)
2
1
0
minus1
210minus1minus2
DF1 (79)
DF2
(21
)
Chapada dos Guimaraes-MTCuiab a-MTNS Livramento-MTPorto Estrela-MTC aceres-MTBarra do Garccedilas-MTPocon e-MTUruaccedilu-GO
Alto Alegre-SP
Primavera-PAItapipoca-CETaBalsas-MABrejo do Piauı-PIacute
ıba-CE
Ic em-SP
(c)
Figure 3 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of 101 males (a) 37 females (b)and six bioacoustic variables (c) of Pseudopaludicola mystacalis from 15 different localities in Brazil
Maximum variation in temporal variables (notes perminute and number of pulses) of the calls of all specimensanalyzed is 2136 notesmin and 8 pulsesnote In the mostdistant known locations the difference in the number of notesper minute and in the number of pulses is 1003 notesmin
and 6 pulsesnote respectively Considering subsets of pop-ulations from Brazilian Northeast and Brazilian Midwestmaximum interpopulational variation is 1146 notesmin and1335 notesmin respectively There are 7 pulsesnote in callsfrom populations of both areas Maximum intrapopulational
Advances in Zoology 9
Pseudopaludicola serrana Pseudopaludicola murundu Pseudopaludicola saltica
05 1 15 2 25 3 35 4 45 5
A B C D E F G H I(k
Hz)
8
7
6
5
4
3
2
1
(s)
Figure 4 Spectrograms (DFT size = 512 samples two notes for each locality) of advertisement calls of Pseudopaludicola serrana (AndashC) andP murundu (DndashF) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais-Uberlandia (G) state of MatoGrosso-Chapada dos Guimaraes (type-locality H) and Porto Estrela (I)
Note Pulses
(a) (b)
(c) (d)
(e) (f)
(g) (h)
Figure 5 Oscillograms of advertisement calls of Pseudopaludicola serrana (a)-(b) and P murundu (c)ndash(e) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais Uberlandia (f) state of Mato Grosso Chapada dos Guimaraes (type-locality (g))and Porto Estrela (h) Total time of each oscillogram corresponds to 05 s
10 Advances in Zoology
4
2
0
minus2
minus4
6420minus2minus4
DF2
(2
)
DF1 (98)
(a)
4
2
0
minus2
minus4
6420minus2minus4
DF2
(1
)
DF1 (99)
(b)
Figure 6 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of males (a) and six bioacousticvariables (b) of Pseudopaludicola murundu (open circles) P saltica (triangles) and P serrana (closed circles)
Elevation (m)
0
(km)
minus155ndash350351ndash700701ndash1050
1050ndash14001401ndash1750
300
N
1
2
3
4
5
6 78
91011
12
13
Figure 7 Geographical distribution of Pseudopaludicola murundu(circles) and P saltica (triangles) in southeastern Brazil state of SaoPaulomdashRioClaro (type locality (1)) andCampinas (2) state ofMinasGeraismdashPocos de Caldas (3) Alpinopolis (4) (see [17]) Sao Roquede Minas (5) Sao Joao Del Rei (6) Mariana (7) Ouro Branco (8)Itabirito (9) Brumadinho (10) Lavras Novas (11) Botumirim (12)and Uberlandia (13)
variation in the number of notes per minute and in thenumber of pulses in four localities from the state of MatoGrosso is 81 notesmin in Cuiaba and 5 pulsesnote in Cuiabaand Nossa Senhora do Livramento (see Table 3 and [8])Mean note duration does not differ significantly in all theexamined calls (Table 3 119865 = 49 df = 2 119875 = 003)
Table 5 Summary of the number of male specimens correctlyclassified as Pseudopaludicolamurundu P saltica or P serrana usingdiscriminant function analysis of 12 morphometric measurementsand seven bioacoustic variables
Morphometric measurementsTrue group
P murundu P saltica P serranaP murundu 1 0 5P saltica 0 39 0P serrana 3 0 19Total number 6 39 22 16 100 86
Bioacoustic variablesTrue group
P murundu P saltica P serranaP murundu 5 0 1P saltica 0 8 1P serrana 3 0 2Total number 6 9 5 83 889 40
Acoustic analysis of geographical variation in specieswith an extent of occurrence of the magnitude seen inP mystacalis sometimes reveals cryptic taxa being treatedunder a single name However this was not the case in Pmystacalis a taxon that remained erroneously characterizedand poorly recognized in the literature until recently [8] Ourresults reveal a relatively small variation in morphologicaland acoustical traits of P mystacalis and allow confirming thepresence of the species in a wide geographical area along theBrazilian open ecosystems
Advances in Zoology 11
Table 6 Ratios of selected measurements (in mm) of males of Pseudopaludicola murundu P salticaand P serrana Values are presented asmean plusmn standard deviation119873 = number of specimens analyzed
HLSVL HWSVL HLHW HALSVL FLSVL THLSVL TLSVLP serrana (119873 = 21) 040 plusmn 003 036 plusmn 002 110 plusmn 006 027 plusmn 002 061 plusmn 004 056 plusmn 003 070 plusmn 003
P murundu (119873 = 5) 039 plusmn 004 035 plusmn 003 111 plusmn 009 027 plusmn 001 066 plusmn 002 056 plusmn 002 070 plusmn 003
P saltica (119873 = 44) 041 plusmn 004 038 plusmn 003 109 plusmn 011 026 plusmn 003 068 plusmn 006 055 plusmn 005 073 plusmn 005
HAL hand length HL head length HW head width FL foot length SVL snout-vent length THL thigh length TL tibia length
42 Taxonomic Status of Pseudopaludicola serrana Toledo2010 When describing P serrana Toledo [15] used asmorphological characteristics separating the three speciesbelonging to the P saltica group the aspect (relative size andcoloration) of nuptial pads in the external part of finger I andaspect of the vocal sac Such characteristics allow differingP serrana and P murundu from P saltica but do not allowdiffering P serrana from P murundu [15] Previously Haddadand Cardoso [17] had called attention to the fact that nuptialpads were more developed in specimens of P saltica from thetype-locality (Chapada do Guimaraes Mato Grosso) than inspecimens collected and recorded in localities in the statesof Minas Gerais and Sao Paulo In the same article Haddadand Cardoso [17] also presented a spectrogram of the callof a specimen from Campinas Sao Paulo Based on suchreported morphological evidence and acoustic parameterswe here argue that specimens from Minas Gerais and SaoPaulo attributed to P saltica in Haddad and Cardoso [17] infact correspond to P murundu
The only external morphological characteristic used byToledo [15] to differ P serrana from P murunduwas a shorterhead lengthheadwidth ratio (HLHW= 097plusmn006 in the fiveindividuals ofP serrana evaluated 111plusmn007 in 11 individualsof P murundu) After having analyzed a higher number ofspecimens attributed to P serrana (119873 = 21) we found thatHLHW (110 plusmn 006 see Table 6) in this sample does notdiffer from the values presented in the original descriptionand confirmed herein for P murundu
The description of P serrana was also based on physicalcharacteristics of its advertisement calls [15] However theoriginal dataset is relatively low 12 notes of a single maleof P saltica 14 notes of 2 males of P murundu and 15notes of 3 males of P serrana were analyzed and comparedOnly one out of four acoustic variables (pulse duration) wasconsidered diagnostic for the new species Toledo [15] alsoshowed that dominant frequency range of P serrana wascompletely nested within the dominant frequency range of Pmurundu However when later proposing the synonymiza-tion of Pseudopaludicola riopiedadensis Mercadal de Bar-rio and Barrio 1994 to Pseudopaludicola ternetzi Miranda-Ribeiro 1937 Cardozo and Toledo [5] based their decision onldquoseveral important overlapsrdquo including dominant frequencyranges between the two species Indeed our data showedthat dominant frequency contributed to higher loadingsto separate species in the P saltica group Nonoverlappingdominant frequencies would therefore be expected betweenrelated but distinct species of Pseudopaludicola
Bioacoustic data have proven to be useful for uncoveringmorphologically cryptic species in the genus Pseudopaludi-cola [4ndash9 15 16] Advertisement calls of species in this genusmight be divided into three distinct groups according to typeof notes nonpulsed notes notes with concatenated pulsesand noteswith nonconcatenated pulses [7] Each groupmightbe diagnosed by temporal (pulses per note note and pulseduration internotes and interpulses intervals note rate andpulse rate) and spectral variables (dominant frequency andharmonics) which in combination allow characterizing allthe species for which calls were already analyzed except forP serrana and P murundu As evidenced by the recent syn-onymization of Pseudopaludicola riopiedadensis to P ternetzi[15] and reinforced herein by the proposed synonymizationof P serrana to P murundu morphologically similar speciesof Pseudopaludicola presenting the same type of note and anoverlap in their spectral acoustic variables are expected torepresent the same taxon Therefore no arguments remainto consider P serrana as a distinct species from P murunduand the former must be considered as a junior synonym of Pmurundu
5 Conclusions
We here report on the variation in morphometric charactersand variation in bioacoustic variables of the advertisementcalls in fifteen Brazilian populations of Pseudopaludicolamys-tacalis Although limited our sample evidenced no statisticaldifferences in any of the evaluated attributes and allowed usto confirm that this species is widely distributed in BrazilMorphometric and bioacoustic data did not differ also inpopulations currently attributed to Pseudopaludicola serranaand Pseudopaludicola murundu and the former taxon ishere considered as a junior synonym of P murundu Thedata in the present work aims at contributing to a betterunderstanding of the diversity and distribution patterns inthe genus Pseudopaludicola
Appendices
A Voucher Specimens Examined
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality 22∘1910158405210158401015840S 47∘4210158405610158401015840W)-F UFMT 18454MUFMT 18395-6 UFMT 18455-7
Pseudopaludicola mystacalis Brazil Para Primavera(00∘5710158402210158401015840S 47∘0710158401210158401015840W)-M UFMT 11651 UFMT 11827
12 Advances in Zoology
UFMT 11833 UFMT 11836 UFMT 11839 Goias Uruacu(14∘3110158403510158401015840S 49∘0710158405410158401015840W)-F UFMT 18397-400 UFMT18458-9 M UFMT 18401-15 UFMT 18458-64 Mato GrossoBarra do Garcas (15∘3110158405710158401015840S 52∘1410158401010158401015840W)-M UFMT11097 UFMT 11307 UFMT 11319 UFMT 11324 Caceres(16∘1710158405910158401015840S 58∘0910158400910158401015840W)-F UFMT 5906 UFMT 5950UFMT 5955 UFMT 5962 UFMT 9152 UFMT 10445UFMT 10448 UFMT 13669 M UFMT 10451-2 UFMT10455 UFMT 10458 UFMT 10466 UFMT 10495 UFMT10506 UFMT 10508 UFMT 13670 Chapada dos Guimaraes(type-locality 14∘5010158403410158401015840S 55∘2310158401010158401015840W)-F UFMT 8109 MUFMT 487 UFMT 817 UFMT 820 UFMT 12890 Cuiaba(15∘3910158403310158401015840S 55∘5610158403010158401015840W)-M UFMT 15980 UFMT 2426UFMT 2430 UFMT 2432 UFMT 2434-7 UFMT 2439UFMT 7399 UFMT 7653 UFMT 8177-8 UFMT 8180UFMT 8182 UFMT 8184-5 UFMT 13671 Nossa Senhorado Livramento (16∘2110158405810158401015840S 56∘1810158403310158401015840W)-F UFMT 18465UFMT 352 UFMT 6436 UFMT 6466-7 UFMT 6488UFMT 6511 M UFMT 4343 UFMT 6487 UFMT 6491UFMT6498UFMT6515Pocone (16∘3010158405810158401015840S 56∘4410158405310158401015840W)-M UFMT 348-50 UFMT 889 UFMT 4316 UFMT 4318UFMT 4321 UFMT 13672 and Porto Estrela (15∘3510158400510158401015840S57∘1310158402010158401015840W)-F UFMT 18466-7 UFMT 138 UFMT 13482M UFMT 18468-9 UFMT 402 UFMT 2200 UFMT 11346Sao Paulo Icem (20∘2010158403110158401015840S 49∘1110158404210158401015840W)-F UFMT 18421UFMT 18470-2 M UFMT 18422-3 UFMT 18473 and AltoAlegre (21∘3310158402010158401015840S 50∘1310158402210158401015840W)-F UFMT 18474-5 UFMT18479 MUFMT 18476-8 UFMT 18480-6
Pseudopaludicola saltica Brazil Mato Grosso Chapadados Guimaraes (type-locality 15∘2310158400910158401015840S 55∘5010158402410158401015840W)-MUFMT 482 UFMT 819 UFMT 821 UFMT 823 UFMT 1433-5 UFMT 1437-41 UFMT 2873 UFMT 2877 UFMT 2880-1F UFMT 1442 Cuiaba M UFMT 270 UFMT 473 UFMT476 UFMT 13657-68 F UFMT 13655-6) Nova Lacerda (MUFMT 13499-501) Porto Estrela Estacao Ecologica da Serradas Araras (M UFMT 561) and Vila Bela da SantıssimaTrindade (M UFMT 4082 UFMT 4112 UFMT 4123 UFMT4147 UFMT4153 UFMT4157 UFMT4172)MatoGrosso doSul Sonora (M UFMT 1147 UFMT 1195)
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho (type-locality 20∘0610158403210158401015840S 43∘5810158405310158401015840W)-F MCNAM 3675 MUFMT 18424 UFMT 18451 MCNAM 3677-8 MCNAM3680 Itabirito (20∘1310158402910158401015840S 43∘4810158404910158401015840W)-F MCNAM14620-1 M MCNAM 14625 Lavras Novas (20∘2810158405710158401015840S43∘3010158405210158401015840W)-F MCNAM 3694 M MCNAM 3695MCNAM 3690 Mariana (20∘0910158401210158401015840S 43∘3010158400210158401015840W)-FMCNAM 6465 M MCNAM 6457 MCNAM 6461-2 OuroBranco (20∘3010158401610158401015840S 43∘4210158400410158401015840W)-M MCNAM 6559 SaoJoao Del Rei (21∘0810158402510158401015840S 44∘1710158403110158401015840W)-M UFMT 18425-6UFMT 18452-3 and Botumirim (16∘4410158401310158401015840S 42∘3410158402910158401015840W)-FMCNAM 6713 M MCNAM 6832 MCNAM 6834 MCNAM6636 MCNAM 6642-3
B Analyzed Sound Files
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality) LH 676 no voucher specimen LH 677 call
fromUFMT 18455 LH 678 call fromUFMT 18395 and FNJV12976 no voucher specimen Minas Gerais Sao Roque deMinas (20∘1310158402010158401015840S 46∘2710158402410158401015840W) FNJV 4575 no voucherspecimen and Pocos de Caldas (21∘5510158400410158401015840S 46∘3410158400210158401015840W)FNJV 4576 no voucher specimen
Pseudopaludicola mystacalis Brazil Ceara Itapipoca(03∘2410158405810158401015840S 39∘4110158403110158401015840W) LH 655 no voucher specimenTaiba (03∘2510158404410158401015840S 38∘5710158404310158401015840W) LH 658 no voucher spec-imen Goias Uruacu LH 639 call from UFMT 18410) MatoGrosso Chapada dos Guimaraes (type-locality) LH 13A-05no voucher specimen) Caceres LH 47A-04 call fromUFMT10451 Cuiaba LH 14A-01 call from UFMT 2426 LH 14A-02 call from UFMT 2424 Pocone LH 01A-01 call fromUFMT 4321 and Nossa Senhora do Livramento LH 04A-10 call from UFMT 4330 Maranhao Balsa (07∘2810158404910158401015840S46∘0310158401910158401015840W) LH 284 no voucher specimen Piauı Brejo doPiauı (08∘1110158405010158401015840S 42∘4910158405910158401015840W) LH 184 call from UFMT11202 Para Primavera LH 352 call from UFMT 11836 SaoPaulo Icem LH 701 call from UFMT 18423
Pseudopaludicola saltica BrazilMatoGrossoCuiaba LH13A-01 call fromUFMT 8187Nova Lacerda LH 42A-06 callfrom UFMT 13499 LH 42A-07 call from UFMT 13500 andPorto Estrela LH 12 no voucher specimen LH 13 call fromUFMT 13678 LH 14 call fromUFMT 16423 LH 16 call fromUFMT 16417 LH 17 call from UFMT 16414 and LH 18 callfrom UFMT 16385 Minas Gerais Uberlandia (18∘5810158403010158401015840S48∘1710158402610158401015840W) LH 709 no voucher specimen
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho LH 673call from UFMT 18451 LH 674 no voucher specimen andSao Joao Del Rei LH 675 call from UFMT 18426 and FNJV12879-80 no voucher specimen
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Special thanks go to Felipe Franco Curcio Diva MariaBorges-Nojosa and Luciana Barreto Nascimento for allow-ing access to the material under their care at ldquoColecaoZoologica de Vertebrados da Universidade Federal de MatoGrossordquo (UFMT) ldquoColecao Herpetologica da UniversidadeFederal do Cearardquo (UFC) and ldquoMuseu de Ciencias Naturaisrdquo(MCNAM Belo Horizonte Minas Gerais) respectively toAdao J Cardoso (in memoriam) and Luis F Toledo for therecordings and for allowing access respectively to bioa-coustic samples deposited at ldquoFonoteca Neotropical JacquesVielliardrdquo (FNJV) to the CNPq project ldquoRede de pesquisa emanfıbios e repteis de ecossistemas nao florestais brasileirosrdquo(Process no 5633522010-8) for logistical support to VivianUhlig (RANICMBio) for estimates of extent of occurrenceAndre Pansonato thanks ldquoCoordenacao de Aperfeicoamentode Pessoal de Nivel Superiorrdquo (CAPES) for a PhD scholar-ship and Christine Strussmann thanks CNPq for a researchfellowship (Process no 3095412012-3)
Advances in Zoology 13
References
[1] K D Wells The Ecology amp Behavior of Amphibians TheUniversity of Chicago Chicago Ill USA 2007
[2] M Vences M Gehara J Kohler and F Glaw ldquoDescription of anewMalagasy treefrog (Boophis) occurring syntopically with itssister species and a plea for studies on non-allopatric speciationin tropical amphibiansrdquo Amphibia Reptilia vol 33 no 3-4 pp503ndash520 2012
[3] I De La Riva R Marquez and J Bosch ldquoDescription ofthe advertisement calls of some South American Hylidae(Amphibia Anura) taxonomic and methodological conse-quencesrdquo Bonner Zoologische Beitrage vol 47 pp 175ndash185 1997
[4] F S de Andrade and T R de Carvalho ldquoA new species of Pseu-dopaludicola Miranda-Ribeiro (Leiuperinae LeptodactylidaeAnura) from the Cerrado of southeastern Brazilrdquo Zootaxa vol3608 no 5 pp 389ndash397 2013
[5] D Cardozo and L F Toledo ldquoTaxonomic status of Pseudopalu-dicola riopiedadensis Mercadal de Barrio and Barrio 1994(Anura Leptodactylidae Leiuperinae)rdquo Zootaxa vol 3734 pp571ndash582 2013
[6] T R de Carvalho ldquoA new species of PseudopaludicolaMiranda-Ribeiro (Leiuperinae Leptodactylidae Anura) from the Cer-rado of southeastern Brazil with a distinctive advertisement callpatternrdquo Zootaxa no 3328 pp 47ndash54 2012
[7] F M Magalhaes D Loebmann M N C Kokubum C F BHaddad and A A Garda ldquoA new species of Pseudopaludi-cola (Anura Leptodactylidae Leiuperinae) from NortheasternBrazilrdquo Herpetologica vol 70 pp 77ndash88 2014
[8] A Pansonato C Strussmann J R Mudrek and I A Mar-tins ldquoMorphometric and bioacoustic data on three species ofPseudopaludicola Miranda-Ribeiro 1926 (Anura Leptodactyl-idae Leiuperinae) described from Chapada dos GuimaraesMato Grosso Brazil with the revalidation of Pseudopaludicolaameghini (Cope 1887)rdquo Zootaxa vol 3620 no 1 pp 147ndash1622013
[9] I J Roberto D Cardozo and R W Avila ldquoA new speciesof Pseudopaludicola (Anura Leiuperidae) from Western PiauıState Northeast Brazilrdquo Zootaxa vol 3636 no 2 pp 348ndash3602013
[10] S B Barreto M S Tinoco D Couto-Ferreira and H CBrowne-Ribeiro ldquoDistribuicao de Pseudopaludicola aff falcipes(Anura Leiuperidae) na restinga do litoral norte da BahiaBrasilrdquoRevista Latino-Americana de Conservacao vol 2 pp 27ndash36 2012
[11] E R Favero A C P Veiga-Menoncello D C Rossa-Feres et alldquoIntrageneric karyotypic variation in Pseudopaludicola (AnuraLeiuperidae) and its taxonomic relatednessrdquo Zoological Studiesvol 50 no 6 pp 826ndash836 2011
[12] M Jansen R Bloch A Schulze andM Pfenninger ldquoIntegrativeinventory of Boliviarsquos lowland anurans reveals hidden diversityrdquoZoologica Scripta vol 40 no 6 pp 567ndash583 2011
[13] C P D Prado M Uetanabaro and C F B Haddad ldquoBreed-ing activity patterns reproductive modes and habitat use byanurans (Amphibia) in a seasonal environment in the PantanalBrazilrdquo Amphibia Reptilia vol 26 no 2 pp 211ndash221 2005
[14] R A Silva I A Martins and D C Rossa-Feres ldquoBioacustica esıtio de vocalizacao em taxocenoses de anfıbios de area abertano Noroeste Paulistardquo Biota Neotropica vol 8 pp 123ndash1342008
[15] L F Toledo ldquoDescription of a new species of PseudopaludicolaMiranda-Ribeiro 1926 from the state of Sao Paulo SoutheasternBrazil (Anura Leiuperidae)rdquoZootaxa no 2681 pp 47ndash56 2010
[16] L F Toledo S Siqueira T CDuarte A C P Veiga-MenoncelloS M Recco-Pimentel and C F B Haddad ldquoDescription of anew species of Pseudopaludicola Miranda-Ribeiro 1926 fromthe state of Sao Paulo Southeastern Brazil (Anura Leiuperi-dae)rdquo Zootaxa no 2496 pp 38ndash48 2010
[17] C F B Haddad and A J Cardoso ldquoTaxonomia de tres especiesde Pseudopaludicola (Anura Leptodactylidae)rdquo Papeis Avulsosde Zoologia vol 36 pp 287ndash300 1987
[18] T C Duarte A C P Veiga-Menoncello J F R Lima et alldquoChromosome analysis in Pseudopaludicola (Anura Leiuperi-dae) with description of sex chromosomes XXXY in P salticardquoHereditas vol 147 no 2 pp 43ndash52 2010
[19] A C P Veiga-Menoncello L B Lourenco C Strussmannet al ldquoA phylogenetic analysis of Pseudopaludicola (Anura)providing evidence of progressive chromosome reductionrdquoZoologica Scripta vol 43 no 3 pp 261ndash272 2014
[20] W R Heyer A S Rand C A G Cruz O L Peixoto and CE Nelson ldquoFrogs of Boraceiardquo Arquivos de Zoologia vol 31 pp231ndash410 1990
[21] W E Duellman The Hylid Frogs of Middle America vol 1 ofMonograph of the Museum of Natural History of University ofKansas 1970
[22] R Development Core Team The R Project for Statistical Com-puting Vienna Austria 2013 httpwwwr-projectorg
[23] P E Vanzolini ldquoEcological and geographical distribution oflizards in Pernambuco Northeastern Brasil (Sauria)rdquo PapeisAvulsos de Zoologia vol 18 no 4 pp 61ndash90 1974
[24] J M Cei ldquoAmphibians of Argentinardquo Monitore ZoologicoItaliano Nuova Serie Monografia vol 2 pp 1ndash609 1980
[25] F Brusquetti and E O Lavilla ldquoLista comentada de los anfibiosde ParaguayrdquoCuadernos deHerpetologıa vol 20 no 2 pp 3ndash792006
[26] I De La Riva J Kohler S Lotters and S Reichle ldquoTenyears of research on Bolivian amphibians updated checklistdistribution taxonomic problems literature and iconographyrdquoRevista Espanola Herpetologica vol 14 pp 19ndash164 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
6 Advances in Zoology
60∘W 50
∘W 40∘W
0∘
10∘S
20∘S
30∘S
0 400
(km)
PA MA
PICE
4
5
6
MT
32
1
1
7
8
910
11
12
SP
GO
N
Figure 1 Geographical variation in the advertisement calls (oscillograms) of Pseudopaludicola mystacalis from twelve localities in sevenBrazilian states Para (PA) Primavera (1) Ceara (CE) Itapipoca (2) Taıba (3)Maranhao (MA) Balsas (4) Piauı (PI) Brejo do Piauı (5) Goias(GO) Uruacu (6) Mato Grosso (MT) Cuiaba (7) Chapada dos Guimaraes (8) Nossa Senhora do Livramento (9) Pocone (10) Caceres (11)Sao Paulo (SP) Icem (12) Total time of each oscillogram corresponds to 02 s
(Figure 3(c)) and higher loadings corresponded to note rate(385) internote interval (295) and note duration (221) Nodistinct groups were formed along the first function axis ofthe DFA
32 Taxonomic Status of Pseudopaludicola serrana Toledo2010 Advertisement calls of Pseudopaludicola serranarecorded at the type-locality (Brumadinho Minas Gerais)and nearly 120 km southwestwards at Serra do LenheiroMinas Gerais were similar to those of topotypes of P
murundu and distinct from topotypes of P saltica bothin spectral and temporal parameters (Figures 4 and 5)The intraspecific variation in bioacoustic parameters ofP murundu and P serrana presented below is based oncalls from topotypical specimens and on calls recorded inadditional localities listed in Appendix B
Advertisement calls of P serranawere composed of seriesof pulsed notes with nonconcatenated pulses Each note con-sisted of 36plusmn06 (range 2ndash5) pulses Mean note duration was82 plusmn 58ms (26ndash131) emitted on average at intervals of 167 plusmn58ms (63ndash288) Mean duration of each pulse was 9 plusmn 3ms
Advances in Zoology 7
Taiba(CE)
Uruaccedilu(GO)
BBuriti(PI)
C aceres
Livramento (MT)(MT)
(MT)(MT)
(MT) Pocon eCGuimaraes
Cuiab a Itapipoca(CE)
Primavera(PA)
Ic em(SP) Balsas
(MA)
(kH
z)8
7
6
5
4
3
2
1
(s)02 04 06 08 1 12 14 16 18 2 22 24 26 28 3 32 34 36 38
ı
Figure 2 Spectrograms (DFT size = 512 samples) of the advertisement calls of Pseudopaludicola mystacalis from twelve localities (two notesfor each locality) in seven Brazilian states (CE Ceara GO Goias MA Maranhao MT Mato Grosso PA Para PI Piauı SP Sao Paulo)
(2ndash18) Interpulse intervals were 16 plusmn 7ms long (4ndash41) Meanfrequency ranged from 40196 plusmn 453Hz to 70986 plusmn 312Hzand mean dominant frequency was 56251 plusmn 212Hz (5168ndash60293) Advertisement calls of Pmurunduwere composed ofseries of pulsed noteswith nonconcatenated pulses Each noteconsisted of 34 plusmn 06 (range 2ndash5) pulses Mean note durationwas 92 plusmn 18ms (33ndash143) emitted on average at intervals of121 plusmn 30ms (69ndash247) Mean duration of each pulse was 10 plusmn3ms (4ndash18) Interpulse intervals were 24plusmn8ms (5ndash54) Meanfrequency ranged from 36285 plusmn 513Hz to 73301 plusmn 355Hzand mean dominant frequency was 55901 plusmn 176Hz (4875ndash62016Hz)
A discriminant function analysis (DFA)withmorphome-tric data revealed that P serrana and P murundu overlappedalong the first function (DF1) ofDFAwhich explained 98ofthe total variation (Figure 6(a)) While the DFA did not sep-arate P serrana from P murundu both were separated froma third species (Pseudopaludicola saltica) whose individualsalso have long hindlimbs Higher loadings corresponded toeye diameter (121) tarsus length (75) and tibia length (46)DFA from bioacoustic data also separated Pseudopaludicolasaltica from P murundu and P serrana (Figure 6(b))The firstfunction (DF1) of DFA explained 99 of the total variationand higher loadings corresponded to dominant frequency(641) and number of pulses per note (61)
DFAofmorphometricmeasurements using all specimensassigned 100 of the individuals of Pseudopaludicola saltica86 of the individuals of P serrana and only 16 of theindividuals of P murundu to the correct species (Table 5)DFA of bioacoustic variables using all recorded males cor-rectly assigned 89 of the specimens of P saltica 83 of thespecimens of P murundu and 40 of P serrana (Table 5) Incontrast DFA with both morphometric and bioacoustic datausing specimens ofP saltica and amixed sample of specimensattributable to either P murundu or P serrana assigned 100of these latter to a single taxon
The overall similarity in morphology and general struc-ture of the call of P murundu and P serrana evidenced bythe results of DFA with 12 morphometric and six bioacous-tic variables strongly support the rejection of the specificstatus of Pseudopaludicola serrana here considered to be a
junior synonym of Pseudopaludicola murundu Geographi-cal distribution of Pseudopaludicola murundu as presentlyrecognized is not anymore restricted to its type-locality [16]but includes instead twelve distinct localities in southeasternBrazil in the states of Minas Gerais and Sao Paulo (Figure 7)
4 Discussion
41 Geographical Variation in Pseudopaludicola mystacalis(Cope 1887) Among the 18 valid species of Pseudopalu-dicola P mystacalis is currently the one with the mostwidespread distribution range Extent of occurrence in Brazilis nearly two million square kilometers encompassing areasin three different ecoregions along all the ldquodiagonal of openformationsrdquo from South America [23] Caatinga Cerradoand Pantanal It is also found in areas of Chaco in Argentina[24] and Paraguay [25] Although plausible the occurrence inBolivian Chaco was based on material that morphologicallyand bioacoustically would correspond to P ameghini [12 26]Habitats where individuals of this species were found includeldquorestingardquo [10 present study] ldquocampo sujordquo in elevatedplateaus of theCerradoDomain and seasonally floodedfieldsin the Pantanal lowlands [8]
Advertisement calls of Pseudopaludicola mystacalis fromdifferent Brazilian localities are composed of series of noteswith concatenated pulses Maximum variation in dominantfrequency of the calls of all specimens analyzed is 8613Hz(from 44789Hz in Cuiaba Mato Grosso to 53402Hz inBalsas Maranhao Table 3) without any evident latitudinalor longitudinal trend Dominant frequency in the mostdistant known locations (Primavera state of Para and Icemstate of Sao Paulo) varied by 3721 Hz Considering subsetsof populations from Brazilian Northeast (states of CearaMaranhao and Piauı) and from Brazilian Midwest (statesof Mato Grosso and Goias) maximum interpopulationalvariation in dominant frequency is 646Hz and 7752Hzrespectively Maximum intrapopulational variation in dom-inant frequency evaluated for four localities in the lowerportion of the speciesrsquo range (Caceres Cuiaba Nossa Senhorado Livramento and Pocone state ofMatoGrosso) is 5168Hzin Cuiaba (see Table 3 and [8])
8 Advances in Zoology
3
2
1
0
minus1
minus2
210minus1minus2minus3
DF2
(37
)
DF1 (63)
(a)
3
2
1
0
minus1
minus2
minus3
3210minus1minus2minus3minus4
DF2
(15
)
DF1 (85)
(b)
2
1
0
minus1
210minus1minus2
DF1 (79)
DF2
(21
)
Chapada dos Guimaraes-MTCuiab a-MTNS Livramento-MTPorto Estrela-MTC aceres-MTBarra do Garccedilas-MTPocon e-MTUruaccedilu-GO
Alto Alegre-SP
Primavera-PAItapipoca-CETaBalsas-MABrejo do Piauı-PIacute
ıba-CE
Ic em-SP
(c)
Figure 3 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of 101 males (a) 37 females (b)and six bioacoustic variables (c) of Pseudopaludicola mystacalis from 15 different localities in Brazil
Maximum variation in temporal variables (notes perminute and number of pulses) of the calls of all specimensanalyzed is 2136 notesmin and 8 pulsesnote In the mostdistant known locations the difference in the number of notesper minute and in the number of pulses is 1003 notesmin
and 6 pulsesnote respectively Considering subsets of pop-ulations from Brazilian Northeast and Brazilian Midwestmaximum interpopulational variation is 1146 notesmin and1335 notesmin respectively There are 7 pulsesnote in callsfrom populations of both areas Maximum intrapopulational
Advances in Zoology 9
Pseudopaludicola serrana Pseudopaludicola murundu Pseudopaludicola saltica
05 1 15 2 25 3 35 4 45 5
A B C D E F G H I(k
Hz)
8
7
6
5
4
3
2
1
(s)
Figure 4 Spectrograms (DFT size = 512 samples two notes for each locality) of advertisement calls of Pseudopaludicola serrana (AndashC) andP murundu (DndashF) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais-Uberlandia (G) state of MatoGrosso-Chapada dos Guimaraes (type-locality H) and Porto Estrela (I)
Note Pulses
(a) (b)
(c) (d)
(e) (f)
(g) (h)
Figure 5 Oscillograms of advertisement calls of Pseudopaludicola serrana (a)-(b) and P murundu (c)ndash(e) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais Uberlandia (f) state of Mato Grosso Chapada dos Guimaraes (type-locality (g))and Porto Estrela (h) Total time of each oscillogram corresponds to 05 s
10 Advances in Zoology
4
2
0
minus2
minus4
6420minus2minus4
DF2
(2
)
DF1 (98)
(a)
4
2
0
minus2
minus4
6420minus2minus4
DF2
(1
)
DF1 (99)
(b)
Figure 6 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of males (a) and six bioacousticvariables (b) of Pseudopaludicola murundu (open circles) P saltica (triangles) and P serrana (closed circles)
Elevation (m)
0
(km)
minus155ndash350351ndash700701ndash1050
1050ndash14001401ndash1750
300
N
1
2
3
4
5
6 78
91011
12
13
Figure 7 Geographical distribution of Pseudopaludicola murundu(circles) and P saltica (triangles) in southeastern Brazil state of SaoPaulomdashRioClaro (type locality (1)) andCampinas (2) state ofMinasGeraismdashPocos de Caldas (3) Alpinopolis (4) (see [17]) Sao Roquede Minas (5) Sao Joao Del Rei (6) Mariana (7) Ouro Branco (8)Itabirito (9) Brumadinho (10) Lavras Novas (11) Botumirim (12)and Uberlandia (13)
variation in the number of notes per minute and in thenumber of pulses in four localities from the state of MatoGrosso is 81 notesmin in Cuiaba and 5 pulsesnote in Cuiabaand Nossa Senhora do Livramento (see Table 3 and [8])Mean note duration does not differ significantly in all theexamined calls (Table 3 119865 = 49 df = 2 119875 = 003)
Table 5 Summary of the number of male specimens correctlyclassified as Pseudopaludicolamurundu P saltica or P serrana usingdiscriminant function analysis of 12 morphometric measurementsand seven bioacoustic variables
Morphometric measurementsTrue group
P murundu P saltica P serranaP murundu 1 0 5P saltica 0 39 0P serrana 3 0 19Total number 6 39 22 16 100 86
Bioacoustic variablesTrue group
P murundu P saltica P serranaP murundu 5 0 1P saltica 0 8 1P serrana 3 0 2Total number 6 9 5 83 889 40
Acoustic analysis of geographical variation in specieswith an extent of occurrence of the magnitude seen inP mystacalis sometimes reveals cryptic taxa being treatedunder a single name However this was not the case in Pmystacalis a taxon that remained erroneously characterizedand poorly recognized in the literature until recently [8] Ourresults reveal a relatively small variation in morphologicaland acoustical traits of P mystacalis and allow confirming thepresence of the species in a wide geographical area along theBrazilian open ecosystems
Advances in Zoology 11
Table 6 Ratios of selected measurements (in mm) of males of Pseudopaludicola murundu P salticaand P serrana Values are presented asmean plusmn standard deviation119873 = number of specimens analyzed
HLSVL HWSVL HLHW HALSVL FLSVL THLSVL TLSVLP serrana (119873 = 21) 040 plusmn 003 036 plusmn 002 110 plusmn 006 027 plusmn 002 061 plusmn 004 056 plusmn 003 070 plusmn 003
P murundu (119873 = 5) 039 plusmn 004 035 plusmn 003 111 plusmn 009 027 plusmn 001 066 plusmn 002 056 plusmn 002 070 plusmn 003
P saltica (119873 = 44) 041 plusmn 004 038 plusmn 003 109 plusmn 011 026 plusmn 003 068 plusmn 006 055 plusmn 005 073 plusmn 005
HAL hand length HL head length HW head width FL foot length SVL snout-vent length THL thigh length TL tibia length
42 Taxonomic Status of Pseudopaludicola serrana Toledo2010 When describing P serrana Toledo [15] used asmorphological characteristics separating the three speciesbelonging to the P saltica group the aspect (relative size andcoloration) of nuptial pads in the external part of finger I andaspect of the vocal sac Such characteristics allow differingP serrana and P murundu from P saltica but do not allowdiffering P serrana from P murundu [15] Previously Haddadand Cardoso [17] had called attention to the fact that nuptialpads were more developed in specimens of P saltica from thetype-locality (Chapada do Guimaraes Mato Grosso) than inspecimens collected and recorded in localities in the statesof Minas Gerais and Sao Paulo In the same article Haddadand Cardoso [17] also presented a spectrogram of the callof a specimen from Campinas Sao Paulo Based on suchreported morphological evidence and acoustic parameterswe here argue that specimens from Minas Gerais and SaoPaulo attributed to P saltica in Haddad and Cardoso [17] infact correspond to P murundu
The only external morphological characteristic used byToledo [15] to differ P serrana from P murunduwas a shorterhead lengthheadwidth ratio (HLHW= 097plusmn006 in the fiveindividuals ofP serrana evaluated 111plusmn007 in 11 individualsof P murundu) After having analyzed a higher number ofspecimens attributed to P serrana (119873 = 21) we found thatHLHW (110 plusmn 006 see Table 6) in this sample does notdiffer from the values presented in the original descriptionand confirmed herein for P murundu
The description of P serrana was also based on physicalcharacteristics of its advertisement calls [15] However theoriginal dataset is relatively low 12 notes of a single maleof P saltica 14 notes of 2 males of P murundu and 15notes of 3 males of P serrana were analyzed and comparedOnly one out of four acoustic variables (pulse duration) wasconsidered diagnostic for the new species Toledo [15] alsoshowed that dominant frequency range of P serrana wascompletely nested within the dominant frequency range of Pmurundu However when later proposing the synonymiza-tion of Pseudopaludicola riopiedadensis Mercadal de Bar-rio and Barrio 1994 to Pseudopaludicola ternetzi Miranda-Ribeiro 1937 Cardozo and Toledo [5] based their decision onldquoseveral important overlapsrdquo including dominant frequencyranges between the two species Indeed our data showedthat dominant frequency contributed to higher loadingsto separate species in the P saltica group Nonoverlappingdominant frequencies would therefore be expected betweenrelated but distinct species of Pseudopaludicola
Bioacoustic data have proven to be useful for uncoveringmorphologically cryptic species in the genus Pseudopaludi-cola [4ndash9 15 16] Advertisement calls of species in this genusmight be divided into three distinct groups according to typeof notes nonpulsed notes notes with concatenated pulsesand noteswith nonconcatenated pulses [7] Each groupmightbe diagnosed by temporal (pulses per note note and pulseduration internotes and interpulses intervals note rate andpulse rate) and spectral variables (dominant frequency andharmonics) which in combination allow characterizing allthe species for which calls were already analyzed except forP serrana and P murundu As evidenced by the recent syn-onymization of Pseudopaludicola riopiedadensis to P ternetzi[15] and reinforced herein by the proposed synonymizationof P serrana to P murundu morphologically similar speciesof Pseudopaludicola presenting the same type of note and anoverlap in their spectral acoustic variables are expected torepresent the same taxon Therefore no arguments remainto consider P serrana as a distinct species from P murunduand the former must be considered as a junior synonym of Pmurundu
5 Conclusions
We here report on the variation in morphometric charactersand variation in bioacoustic variables of the advertisementcalls in fifteen Brazilian populations of Pseudopaludicolamys-tacalis Although limited our sample evidenced no statisticaldifferences in any of the evaluated attributes and allowed usto confirm that this species is widely distributed in BrazilMorphometric and bioacoustic data did not differ also inpopulations currently attributed to Pseudopaludicola serranaand Pseudopaludicola murundu and the former taxon ishere considered as a junior synonym of P murundu Thedata in the present work aims at contributing to a betterunderstanding of the diversity and distribution patterns inthe genus Pseudopaludicola
Appendices
A Voucher Specimens Examined
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality 22∘1910158405210158401015840S 47∘4210158405610158401015840W)-F UFMT 18454MUFMT 18395-6 UFMT 18455-7
Pseudopaludicola mystacalis Brazil Para Primavera(00∘5710158402210158401015840S 47∘0710158401210158401015840W)-M UFMT 11651 UFMT 11827
12 Advances in Zoology
UFMT 11833 UFMT 11836 UFMT 11839 Goias Uruacu(14∘3110158403510158401015840S 49∘0710158405410158401015840W)-F UFMT 18397-400 UFMT18458-9 M UFMT 18401-15 UFMT 18458-64 Mato GrossoBarra do Garcas (15∘3110158405710158401015840S 52∘1410158401010158401015840W)-M UFMT11097 UFMT 11307 UFMT 11319 UFMT 11324 Caceres(16∘1710158405910158401015840S 58∘0910158400910158401015840W)-F UFMT 5906 UFMT 5950UFMT 5955 UFMT 5962 UFMT 9152 UFMT 10445UFMT 10448 UFMT 13669 M UFMT 10451-2 UFMT10455 UFMT 10458 UFMT 10466 UFMT 10495 UFMT10506 UFMT 10508 UFMT 13670 Chapada dos Guimaraes(type-locality 14∘5010158403410158401015840S 55∘2310158401010158401015840W)-F UFMT 8109 MUFMT 487 UFMT 817 UFMT 820 UFMT 12890 Cuiaba(15∘3910158403310158401015840S 55∘5610158403010158401015840W)-M UFMT 15980 UFMT 2426UFMT 2430 UFMT 2432 UFMT 2434-7 UFMT 2439UFMT 7399 UFMT 7653 UFMT 8177-8 UFMT 8180UFMT 8182 UFMT 8184-5 UFMT 13671 Nossa Senhorado Livramento (16∘2110158405810158401015840S 56∘1810158403310158401015840W)-F UFMT 18465UFMT 352 UFMT 6436 UFMT 6466-7 UFMT 6488UFMT 6511 M UFMT 4343 UFMT 6487 UFMT 6491UFMT6498UFMT6515Pocone (16∘3010158405810158401015840S 56∘4410158405310158401015840W)-M UFMT 348-50 UFMT 889 UFMT 4316 UFMT 4318UFMT 4321 UFMT 13672 and Porto Estrela (15∘3510158400510158401015840S57∘1310158402010158401015840W)-F UFMT 18466-7 UFMT 138 UFMT 13482M UFMT 18468-9 UFMT 402 UFMT 2200 UFMT 11346Sao Paulo Icem (20∘2010158403110158401015840S 49∘1110158404210158401015840W)-F UFMT 18421UFMT 18470-2 M UFMT 18422-3 UFMT 18473 and AltoAlegre (21∘3310158402010158401015840S 50∘1310158402210158401015840W)-F UFMT 18474-5 UFMT18479 MUFMT 18476-8 UFMT 18480-6
Pseudopaludicola saltica Brazil Mato Grosso Chapadados Guimaraes (type-locality 15∘2310158400910158401015840S 55∘5010158402410158401015840W)-MUFMT 482 UFMT 819 UFMT 821 UFMT 823 UFMT 1433-5 UFMT 1437-41 UFMT 2873 UFMT 2877 UFMT 2880-1F UFMT 1442 Cuiaba M UFMT 270 UFMT 473 UFMT476 UFMT 13657-68 F UFMT 13655-6) Nova Lacerda (MUFMT 13499-501) Porto Estrela Estacao Ecologica da Serradas Araras (M UFMT 561) and Vila Bela da SantıssimaTrindade (M UFMT 4082 UFMT 4112 UFMT 4123 UFMT4147 UFMT4153 UFMT4157 UFMT4172)MatoGrosso doSul Sonora (M UFMT 1147 UFMT 1195)
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho (type-locality 20∘0610158403210158401015840S 43∘5810158405310158401015840W)-F MCNAM 3675 MUFMT 18424 UFMT 18451 MCNAM 3677-8 MCNAM3680 Itabirito (20∘1310158402910158401015840S 43∘4810158404910158401015840W)-F MCNAM14620-1 M MCNAM 14625 Lavras Novas (20∘2810158405710158401015840S43∘3010158405210158401015840W)-F MCNAM 3694 M MCNAM 3695MCNAM 3690 Mariana (20∘0910158401210158401015840S 43∘3010158400210158401015840W)-FMCNAM 6465 M MCNAM 6457 MCNAM 6461-2 OuroBranco (20∘3010158401610158401015840S 43∘4210158400410158401015840W)-M MCNAM 6559 SaoJoao Del Rei (21∘0810158402510158401015840S 44∘1710158403110158401015840W)-M UFMT 18425-6UFMT 18452-3 and Botumirim (16∘4410158401310158401015840S 42∘3410158402910158401015840W)-FMCNAM 6713 M MCNAM 6832 MCNAM 6834 MCNAM6636 MCNAM 6642-3
B Analyzed Sound Files
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality) LH 676 no voucher specimen LH 677 call
fromUFMT 18455 LH 678 call fromUFMT 18395 and FNJV12976 no voucher specimen Minas Gerais Sao Roque deMinas (20∘1310158402010158401015840S 46∘2710158402410158401015840W) FNJV 4575 no voucherspecimen and Pocos de Caldas (21∘5510158400410158401015840S 46∘3410158400210158401015840W)FNJV 4576 no voucher specimen
Pseudopaludicola mystacalis Brazil Ceara Itapipoca(03∘2410158405810158401015840S 39∘4110158403110158401015840W) LH 655 no voucher specimenTaiba (03∘2510158404410158401015840S 38∘5710158404310158401015840W) LH 658 no voucher spec-imen Goias Uruacu LH 639 call from UFMT 18410) MatoGrosso Chapada dos Guimaraes (type-locality) LH 13A-05no voucher specimen) Caceres LH 47A-04 call fromUFMT10451 Cuiaba LH 14A-01 call from UFMT 2426 LH 14A-02 call from UFMT 2424 Pocone LH 01A-01 call fromUFMT 4321 and Nossa Senhora do Livramento LH 04A-10 call from UFMT 4330 Maranhao Balsa (07∘2810158404910158401015840S46∘0310158401910158401015840W) LH 284 no voucher specimen Piauı Brejo doPiauı (08∘1110158405010158401015840S 42∘4910158405910158401015840W) LH 184 call from UFMT11202 Para Primavera LH 352 call from UFMT 11836 SaoPaulo Icem LH 701 call from UFMT 18423
Pseudopaludicola saltica BrazilMatoGrossoCuiaba LH13A-01 call fromUFMT 8187Nova Lacerda LH 42A-06 callfrom UFMT 13499 LH 42A-07 call from UFMT 13500 andPorto Estrela LH 12 no voucher specimen LH 13 call fromUFMT 13678 LH 14 call fromUFMT 16423 LH 16 call fromUFMT 16417 LH 17 call from UFMT 16414 and LH 18 callfrom UFMT 16385 Minas Gerais Uberlandia (18∘5810158403010158401015840S48∘1710158402610158401015840W) LH 709 no voucher specimen
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho LH 673call from UFMT 18451 LH 674 no voucher specimen andSao Joao Del Rei LH 675 call from UFMT 18426 and FNJV12879-80 no voucher specimen
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Special thanks go to Felipe Franco Curcio Diva MariaBorges-Nojosa and Luciana Barreto Nascimento for allow-ing access to the material under their care at ldquoColecaoZoologica de Vertebrados da Universidade Federal de MatoGrossordquo (UFMT) ldquoColecao Herpetologica da UniversidadeFederal do Cearardquo (UFC) and ldquoMuseu de Ciencias Naturaisrdquo(MCNAM Belo Horizonte Minas Gerais) respectively toAdao J Cardoso (in memoriam) and Luis F Toledo for therecordings and for allowing access respectively to bioa-coustic samples deposited at ldquoFonoteca Neotropical JacquesVielliardrdquo (FNJV) to the CNPq project ldquoRede de pesquisa emanfıbios e repteis de ecossistemas nao florestais brasileirosrdquo(Process no 5633522010-8) for logistical support to VivianUhlig (RANICMBio) for estimates of extent of occurrenceAndre Pansonato thanks ldquoCoordenacao de Aperfeicoamentode Pessoal de Nivel Superiorrdquo (CAPES) for a PhD scholar-ship and Christine Strussmann thanks CNPq for a researchfellowship (Process no 3095412012-3)
Advances in Zoology 13
References
[1] K D Wells The Ecology amp Behavior of Amphibians TheUniversity of Chicago Chicago Ill USA 2007
[2] M Vences M Gehara J Kohler and F Glaw ldquoDescription of anewMalagasy treefrog (Boophis) occurring syntopically with itssister species and a plea for studies on non-allopatric speciationin tropical amphibiansrdquo Amphibia Reptilia vol 33 no 3-4 pp503ndash520 2012
[3] I De La Riva R Marquez and J Bosch ldquoDescription ofthe advertisement calls of some South American Hylidae(Amphibia Anura) taxonomic and methodological conse-quencesrdquo Bonner Zoologische Beitrage vol 47 pp 175ndash185 1997
[4] F S de Andrade and T R de Carvalho ldquoA new species of Pseu-dopaludicola Miranda-Ribeiro (Leiuperinae LeptodactylidaeAnura) from the Cerrado of southeastern Brazilrdquo Zootaxa vol3608 no 5 pp 389ndash397 2013
[5] D Cardozo and L F Toledo ldquoTaxonomic status of Pseudopalu-dicola riopiedadensis Mercadal de Barrio and Barrio 1994(Anura Leptodactylidae Leiuperinae)rdquo Zootaxa vol 3734 pp571ndash582 2013
[6] T R de Carvalho ldquoA new species of PseudopaludicolaMiranda-Ribeiro (Leiuperinae Leptodactylidae Anura) from the Cer-rado of southeastern Brazil with a distinctive advertisement callpatternrdquo Zootaxa no 3328 pp 47ndash54 2012
[7] F M Magalhaes D Loebmann M N C Kokubum C F BHaddad and A A Garda ldquoA new species of Pseudopaludi-cola (Anura Leptodactylidae Leiuperinae) from NortheasternBrazilrdquo Herpetologica vol 70 pp 77ndash88 2014
[8] A Pansonato C Strussmann J R Mudrek and I A Mar-tins ldquoMorphometric and bioacoustic data on three species ofPseudopaludicola Miranda-Ribeiro 1926 (Anura Leptodactyl-idae Leiuperinae) described from Chapada dos GuimaraesMato Grosso Brazil with the revalidation of Pseudopaludicolaameghini (Cope 1887)rdquo Zootaxa vol 3620 no 1 pp 147ndash1622013
[9] I J Roberto D Cardozo and R W Avila ldquoA new speciesof Pseudopaludicola (Anura Leiuperidae) from Western PiauıState Northeast Brazilrdquo Zootaxa vol 3636 no 2 pp 348ndash3602013
[10] S B Barreto M S Tinoco D Couto-Ferreira and H CBrowne-Ribeiro ldquoDistribuicao de Pseudopaludicola aff falcipes(Anura Leiuperidae) na restinga do litoral norte da BahiaBrasilrdquoRevista Latino-Americana de Conservacao vol 2 pp 27ndash36 2012
[11] E R Favero A C P Veiga-Menoncello D C Rossa-Feres et alldquoIntrageneric karyotypic variation in Pseudopaludicola (AnuraLeiuperidae) and its taxonomic relatednessrdquo Zoological Studiesvol 50 no 6 pp 826ndash836 2011
[12] M Jansen R Bloch A Schulze andM Pfenninger ldquoIntegrativeinventory of Boliviarsquos lowland anurans reveals hidden diversityrdquoZoologica Scripta vol 40 no 6 pp 567ndash583 2011
[13] C P D Prado M Uetanabaro and C F B Haddad ldquoBreed-ing activity patterns reproductive modes and habitat use byanurans (Amphibia) in a seasonal environment in the PantanalBrazilrdquo Amphibia Reptilia vol 26 no 2 pp 211ndash221 2005
[14] R A Silva I A Martins and D C Rossa-Feres ldquoBioacustica esıtio de vocalizacao em taxocenoses de anfıbios de area abertano Noroeste Paulistardquo Biota Neotropica vol 8 pp 123ndash1342008
[15] L F Toledo ldquoDescription of a new species of PseudopaludicolaMiranda-Ribeiro 1926 from the state of Sao Paulo SoutheasternBrazil (Anura Leiuperidae)rdquoZootaxa no 2681 pp 47ndash56 2010
[16] L F Toledo S Siqueira T CDuarte A C P Veiga-MenoncelloS M Recco-Pimentel and C F B Haddad ldquoDescription of anew species of Pseudopaludicola Miranda-Ribeiro 1926 fromthe state of Sao Paulo Southeastern Brazil (Anura Leiuperi-dae)rdquo Zootaxa no 2496 pp 38ndash48 2010
[17] C F B Haddad and A J Cardoso ldquoTaxonomia de tres especiesde Pseudopaludicola (Anura Leptodactylidae)rdquo Papeis Avulsosde Zoologia vol 36 pp 287ndash300 1987
[18] T C Duarte A C P Veiga-Menoncello J F R Lima et alldquoChromosome analysis in Pseudopaludicola (Anura Leiuperi-dae) with description of sex chromosomes XXXY in P salticardquoHereditas vol 147 no 2 pp 43ndash52 2010
[19] A C P Veiga-Menoncello L B Lourenco C Strussmannet al ldquoA phylogenetic analysis of Pseudopaludicola (Anura)providing evidence of progressive chromosome reductionrdquoZoologica Scripta vol 43 no 3 pp 261ndash272 2014
[20] W R Heyer A S Rand C A G Cruz O L Peixoto and CE Nelson ldquoFrogs of Boraceiardquo Arquivos de Zoologia vol 31 pp231ndash410 1990
[21] W E Duellman The Hylid Frogs of Middle America vol 1 ofMonograph of the Museum of Natural History of University ofKansas 1970
[22] R Development Core Team The R Project for Statistical Com-puting Vienna Austria 2013 httpwwwr-projectorg
[23] P E Vanzolini ldquoEcological and geographical distribution oflizards in Pernambuco Northeastern Brasil (Sauria)rdquo PapeisAvulsos de Zoologia vol 18 no 4 pp 61ndash90 1974
[24] J M Cei ldquoAmphibians of Argentinardquo Monitore ZoologicoItaliano Nuova Serie Monografia vol 2 pp 1ndash609 1980
[25] F Brusquetti and E O Lavilla ldquoLista comentada de los anfibiosde ParaguayrdquoCuadernos deHerpetologıa vol 20 no 2 pp 3ndash792006
[26] I De La Riva J Kohler S Lotters and S Reichle ldquoTenyears of research on Bolivian amphibians updated checklistdistribution taxonomic problems literature and iconographyrdquoRevista Espanola Herpetologica vol 14 pp 19ndash164 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
Advances in Zoology 7
Taiba(CE)
Uruaccedilu(GO)
BBuriti(PI)
C aceres
Livramento (MT)(MT)
(MT)(MT)
(MT) Pocon eCGuimaraes
Cuiab a Itapipoca(CE)
Primavera(PA)
Ic em(SP) Balsas
(MA)
(kH
z)8
7
6
5
4
3
2
1
(s)02 04 06 08 1 12 14 16 18 2 22 24 26 28 3 32 34 36 38
ı
Figure 2 Spectrograms (DFT size = 512 samples) of the advertisement calls of Pseudopaludicola mystacalis from twelve localities (two notesfor each locality) in seven Brazilian states (CE Ceara GO Goias MA Maranhao MT Mato Grosso PA Para PI Piauı SP Sao Paulo)
(2ndash18) Interpulse intervals were 16 plusmn 7ms long (4ndash41) Meanfrequency ranged from 40196 plusmn 453Hz to 70986 plusmn 312Hzand mean dominant frequency was 56251 plusmn 212Hz (5168ndash60293) Advertisement calls of Pmurunduwere composed ofseries of pulsed noteswith nonconcatenated pulses Each noteconsisted of 34 plusmn 06 (range 2ndash5) pulses Mean note durationwas 92 plusmn 18ms (33ndash143) emitted on average at intervals of121 plusmn 30ms (69ndash247) Mean duration of each pulse was 10 plusmn3ms (4ndash18) Interpulse intervals were 24plusmn8ms (5ndash54) Meanfrequency ranged from 36285 plusmn 513Hz to 73301 plusmn 355Hzand mean dominant frequency was 55901 plusmn 176Hz (4875ndash62016Hz)
A discriminant function analysis (DFA)withmorphome-tric data revealed that P serrana and P murundu overlappedalong the first function (DF1) ofDFAwhich explained 98ofthe total variation (Figure 6(a)) While the DFA did not sep-arate P serrana from P murundu both were separated froma third species (Pseudopaludicola saltica) whose individualsalso have long hindlimbs Higher loadings corresponded toeye diameter (121) tarsus length (75) and tibia length (46)DFA from bioacoustic data also separated Pseudopaludicolasaltica from P murundu and P serrana (Figure 6(b))The firstfunction (DF1) of DFA explained 99 of the total variationand higher loadings corresponded to dominant frequency(641) and number of pulses per note (61)
DFAofmorphometricmeasurements using all specimensassigned 100 of the individuals of Pseudopaludicola saltica86 of the individuals of P serrana and only 16 of theindividuals of P murundu to the correct species (Table 5)DFA of bioacoustic variables using all recorded males cor-rectly assigned 89 of the specimens of P saltica 83 of thespecimens of P murundu and 40 of P serrana (Table 5) Incontrast DFA with both morphometric and bioacoustic datausing specimens ofP saltica and amixed sample of specimensattributable to either P murundu or P serrana assigned 100of these latter to a single taxon
The overall similarity in morphology and general struc-ture of the call of P murundu and P serrana evidenced bythe results of DFA with 12 morphometric and six bioacous-tic variables strongly support the rejection of the specificstatus of Pseudopaludicola serrana here considered to be a
junior synonym of Pseudopaludicola murundu Geographi-cal distribution of Pseudopaludicola murundu as presentlyrecognized is not anymore restricted to its type-locality [16]but includes instead twelve distinct localities in southeasternBrazil in the states of Minas Gerais and Sao Paulo (Figure 7)
4 Discussion
41 Geographical Variation in Pseudopaludicola mystacalis(Cope 1887) Among the 18 valid species of Pseudopalu-dicola P mystacalis is currently the one with the mostwidespread distribution range Extent of occurrence in Brazilis nearly two million square kilometers encompassing areasin three different ecoregions along all the ldquodiagonal of openformationsrdquo from South America [23] Caatinga Cerradoand Pantanal It is also found in areas of Chaco in Argentina[24] and Paraguay [25] Although plausible the occurrence inBolivian Chaco was based on material that morphologicallyand bioacoustically would correspond to P ameghini [12 26]Habitats where individuals of this species were found includeldquorestingardquo [10 present study] ldquocampo sujordquo in elevatedplateaus of theCerradoDomain and seasonally floodedfieldsin the Pantanal lowlands [8]
Advertisement calls of Pseudopaludicola mystacalis fromdifferent Brazilian localities are composed of series of noteswith concatenated pulses Maximum variation in dominantfrequency of the calls of all specimens analyzed is 8613Hz(from 44789Hz in Cuiaba Mato Grosso to 53402Hz inBalsas Maranhao Table 3) without any evident latitudinalor longitudinal trend Dominant frequency in the mostdistant known locations (Primavera state of Para and Icemstate of Sao Paulo) varied by 3721 Hz Considering subsetsof populations from Brazilian Northeast (states of CearaMaranhao and Piauı) and from Brazilian Midwest (statesof Mato Grosso and Goias) maximum interpopulationalvariation in dominant frequency is 646Hz and 7752Hzrespectively Maximum intrapopulational variation in dom-inant frequency evaluated for four localities in the lowerportion of the speciesrsquo range (Caceres Cuiaba Nossa Senhorado Livramento and Pocone state ofMatoGrosso) is 5168Hzin Cuiaba (see Table 3 and [8])
8 Advances in Zoology
3
2
1
0
minus1
minus2
210minus1minus2minus3
DF2
(37
)
DF1 (63)
(a)
3
2
1
0
minus1
minus2
minus3
3210minus1minus2minus3minus4
DF2
(15
)
DF1 (85)
(b)
2
1
0
minus1
210minus1minus2
DF1 (79)
DF2
(21
)
Chapada dos Guimaraes-MTCuiab a-MTNS Livramento-MTPorto Estrela-MTC aceres-MTBarra do Garccedilas-MTPocon e-MTUruaccedilu-GO
Alto Alegre-SP
Primavera-PAItapipoca-CETaBalsas-MABrejo do Piauı-PIacute
ıba-CE
Ic em-SP
(c)
Figure 3 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of 101 males (a) 37 females (b)and six bioacoustic variables (c) of Pseudopaludicola mystacalis from 15 different localities in Brazil
Maximum variation in temporal variables (notes perminute and number of pulses) of the calls of all specimensanalyzed is 2136 notesmin and 8 pulsesnote In the mostdistant known locations the difference in the number of notesper minute and in the number of pulses is 1003 notesmin
and 6 pulsesnote respectively Considering subsets of pop-ulations from Brazilian Northeast and Brazilian Midwestmaximum interpopulational variation is 1146 notesmin and1335 notesmin respectively There are 7 pulsesnote in callsfrom populations of both areas Maximum intrapopulational
Advances in Zoology 9
Pseudopaludicola serrana Pseudopaludicola murundu Pseudopaludicola saltica
05 1 15 2 25 3 35 4 45 5
A B C D E F G H I(k
Hz)
8
7
6
5
4
3
2
1
(s)
Figure 4 Spectrograms (DFT size = 512 samples two notes for each locality) of advertisement calls of Pseudopaludicola serrana (AndashC) andP murundu (DndashF) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais-Uberlandia (G) state of MatoGrosso-Chapada dos Guimaraes (type-locality H) and Porto Estrela (I)
Note Pulses
(a) (b)
(c) (d)
(e) (f)
(g) (h)
Figure 5 Oscillograms of advertisement calls of Pseudopaludicola serrana (a)-(b) and P murundu (c)ndash(e) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais Uberlandia (f) state of Mato Grosso Chapada dos Guimaraes (type-locality (g))and Porto Estrela (h) Total time of each oscillogram corresponds to 05 s
10 Advances in Zoology
4
2
0
minus2
minus4
6420minus2minus4
DF2
(2
)
DF1 (98)
(a)
4
2
0
minus2
minus4
6420minus2minus4
DF2
(1
)
DF1 (99)
(b)
Figure 6 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of males (a) and six bioacousticvariables (b) of Pseudopaludicola murundu (open circles) P saltica (triangles) and P serrana (closed circles)
Elevation (m)
0
(km)
minus155ndash350351ndash700701ndash1050
1050ndash14001401ndash1750
300
N
1
2
3
4
5
6 78
91011
12
13
Figure 7 Geographical distribution of Pseudopaludicola murundu(circles) and P saltica (triangles) in southeastern Brazil state of SaoPaulomdashRioClaro (type locality (1)) andCampinas (2) state ofMinasGeraismdashPocos de Caldas (3) Alpinopolis (4) (see [17]) Sao Roquede Minas (5) Sao Joao Del Rei (6) Mariana (7) Ouro Branco (8)Itabirito (9) Brumadinho (10) Lavras Novas (11) Botumirim (12)and Uberlandia (13)
variation in the number of notes per minute and in thenumber of pulses in four localities from the state of MatoGrosso is 81 notesmin in Cuiaba and 5 pulsesnote in Cuiabaand Nossa Senhora do Livramento (see Table 3 and [8])Mean note duration does not differ significantly in all theexamined calls (Table 3 119865 = 49 df = 2 119875 = 003)
Table 5 Summary of the number of male specimens correctlyclassified as Pseudopaludicolamurundu P saltica or P serrana usingdiscriminant function analysis of 12 morphometric measurementsand seven bioacoustic variables
Morphometric measurementsTrue group
P murundu P saltica P serranaP murundu 1 0 5P saltica 0 39 0P serrana 3 0 19Total number 6 39 22 16 100 86
Bioacoustic variablesTrue group
P murundu P saltica P serranaP murundu 5 0 1P saltica 0 8 1P serrana 3 0 2Total number 6 9 5 83 889 40
Acoustic analysis of geographical variation in specieswith an extent of occurrence of the magnitude seen inP mystacalis sometimes reveals cryptic taxa being treatedunder a single name However this was not the case in Pmystacalis a taxon that remained erroneously characterizedand poorly recognized in the literature until recently [8] Ourresults reveal a relatively small variation in morphologicaland acoustical traits of P mystacalis and allow confirming thepresence of the species in a wide geographical area along theBrazilian open ecosystems
Advances in Zoology 11
Table 6 Ratios of selected measurements (in mm) of males of Pseudopaludicola murundu P salticaand P serrana Values are presented asmean plusmn standard deviation119873 = number of specimens analyzed
HLSVL HWSVL HLHW HALSVL FLSVL THLSVL TLSVLP serrana (119873 = 21) 040 plusmn 003 036 plusmn 002 110 plusmn 006 027 plusmn 002 061 plusmn 004 056 plusmn 003 070 plusmn 003
P murundu (119873 = 5) 039 plusmn 004 035 plusmn 003 111 plusmn 009 027 plusmn 001 066 plusmn 002 056 plusmn 002 070 plusmn 003
P saltica (119873 = 44) 041 plusmn 004 038 plusmn 003 109 plusmn 011 026 plusmn 003 068 plusmn 006 055 plusmn 005 073 plusmn 005
HAL hand length HL head length HW head width FL foot length SVL snout-vent length THL thigh length TL tibia length
42 Taxonomic Status of Pseudopaludicola serrana Toledo2010 When describing P serrana Toledo [15] used asmorphological characteristics separating the three speciesbelonging to the P saltica group the aspect (relative size andcoloration) of nuptial pads in the external part of finger I andaspect of the vocal sac Such characteristics allow differingP serrana and P murundu from P saltica but do not allowdiffering P serrana from P murundu [15] Previously Haddadand Cardoso [17] had called attention to the fact that nuptialpads were more developed in specimens of P saltica from thetype-locality (Chapada do Guimaraes Mato Grosso) than inspecimens collected and recorded in localities in the statesof Minas Gerais and Sao Paulo In the same article Haddadand Cardoso [17] also presented a spectrogram of the callof a specimen from Campinas Sao Paulo Based on suchreported morphological evidence and acoustic parameterswe here argue that specimens from Minas Gerais and SaoPaulo attributed to P saltica in Haddad and Cardoso [17] infact correspond to P murundu
The only external morphological characteristic used byToledo [15] to differ P serrana from P murunduwas a shorterhead lengthheadwidth ratio (HLHW= 097plusmn006 in the fiveindividuals ofP serrana evaluated 111plusmn007 in 11 individualsof P murundu) After having analyzed a higher number ofspecimens attributed to P serrana (119873 = 21) we found thatHLHW (110 plusmn 006 see Table 6) in this sample does notdiffer from the values presented in the original descriptionand confirmed herein for P murundu
The description of P serrana was also based on physicalcharacteristics of its advertisement calls [15] However theoriginal dataset is relatively low 12 notes of a single maleof P saltica 14 notes of 2 males of P murundu and 15notes of 3 males of P serrana were analyzed and comparedOnly one out of four acoustic variables (pulse duration) wasconsidered diagnostic for the new species Toledo [15] alsoshowed that dominant frequency range of P serrana wascompletely nested within the dominant frequency range of Pmurundu However when later proposing the synonymiza-tion of Pseudopaludicola riopiedadensis Mercadal de Bar-rio and Barrio 1994 to Pseudopaludicola ternetzi Miranda-Ribeiro 1937 Cardozo and Toledo [5] based their decision onldquoseveral important overlapsrdquo including dominant frequencyranges between the two species Indeed our data showedthat dominant frequency contributed to higher loadingsto separate species in the P saltica group Nonoverlappingdominant frequencies would therefore be expected betweenrelated but distinct species of Pseudopaludicola
Bioacoustic data have proven to be useful for uncoveringmorphologically cryptic species in the genus Pseudopaludi-cola [4ndash9 15 16] Advertisement calls of species in this genusmight be divided into three distinct groups according to typeof notes nonpulsed notes notes with concatenated pulsesand noteswith nonconcatenated pulses [7] Each groupmightbe diagnosed by temporal (pulses per note note and pulseduration internotes and interpulses intervals note rate andpulse rate) and spectral variables (dominant frequency andharmonics) which in combination allow characterizing allthe species for which calls were already analyzed except forP serrana and P murundu As evidenced by the recent syn-onymization of Pseudopaludicola riopiedadensis to P ternetzi[15] and reinforced herein by the proposed synonymizationof P serrana to P murundu morphologically similar speciesof Pseudopaludicola presenting the same type of note and anoverlap in their spectral acoustic variables are expected torepresent the same taxon Therefore no arguments remainto consider P serrana as a distinct species from P murunduand the former must be considered as a junior synonym of Pmurundu
5 Conclusions
We here report on the variation in morphometric charactersand variation in bioacoustic variables of the advertisementcalls in fifteen Brazilian populations of Pseudopaludicolamys-tacalis Although limited our sample evidenced no statisticaldifferences in any of the evaluated attributes and allowed usto confirm that this species is widely distributed in BrazilMorphometric and bioacoustic data did not differ also inpopulations currently attributed to Pseudopaludicola serranaand Pseudopaludicola murundu and the former taxon ishere considered as a junior synonym of P murundu Thedata in the present work aims at contributing to a betterunderstanding of the diversity and distribution patterns inthe genus Pseudopaludicola
Appendices
A Voucher Specimens Examined
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality 22∘1910158405210158401015840S 47∘4210158405610158401015840W)-F UFMT 18454MUFMT 18395-6 UFMT 18455-7
Pseudopaludicola mystacalis Brazil Para Primavera(00∘5710158402210158401015840S 47∘0710158401210158401015840W)-M UFMT 11651 UFMT 11827
12 Advances in Zoology
UFMT 11833 UFMT 11836 UFMT 11839 Goias Uruacu(14∘3110158403510158401015840S 49∘0710158405410158401015840W)-F UFMT 18397-400 UFMT18458-9 M UFMT 18401-15 UFMT 18458-64 Mato GrossoBarra do Garcas (15∘3110158405710158401015840S 52∘1410158401010158401015840W)-M UFMT11097 UFMT 11307 UFMT 11319 UFMT 11324 Caceres(16∘1710158405910158401015840S 58∘0910158400910158401015840W)-F UFMT 5906 UFMT 5950UFMT 5955 UFMT 5962 UFMT 9152 UFMT 10445UFMT 10448 UFMT 13669 M UFMT 10451-2 UFMT10455 UFMT 10458 UFMT 10466 UFMT 10495 UFMT10506 UFMT 10508 UFMT 13670 Chapada dos Guimaraes(type-locality 14∘5010158403410158401015840S 55∘2310158401010158401015840W)-F UFMT 8109 MUFMT 487 UFMT 817 UFMT 820 UFMT 12890 Cuiaba(15∘3910158403310158401015840S 55∘5610158403010158401015840W)-M UFMT 15980 UFMT 2426UFMT 2430 UFMT 2432 UFMT 2434-7 UFMT 2439UFMT 7399 UFMT 7653 UFMT 8177-8 UFMT 8180UFMT 8182 UFMT 8184-5 UFMT 13671 Nossa Senhorado Livramento (16∘2110158405810158401015840S 56∘1810158403310158401015840W)-F UFMT 18465UFMT 352 UFMT 6436 UFMT 6466-7 UFMT 6488UFMT 6511 M UFMT 4343 UFMT 6487 UFMT 6491UFMT6498UFMT6515Pocone (16∘3010158405810158401015840S 56∘4410158405310158401015840W)-M UFMT 348-50 UFMT 889 UFMT 4316 UFMT 4318UFMT 4321 UFMT 13672 and Porto Estrela (15∘3510158400510158401015840S57∘1310158402010158401015840W)-F UFMT 18466-7 UFMT 138 UFMT 13482M UFMT 18468-9 UFMT 402 UFMT 2200 UFMT 11346Sao Paulo Icem (20∘2010158403110158401015840S 49∘1110158404210158401015840W)-F UFMT 18421UFMT 18470-2 M UFMT 18422-3 UFMT 18473 and AltoAlegre (21∘3310158402010158401015840S 50∘1310158402210158401015840W)-F UFMT 18474-5 UFMT18479 MUFMT 18476-8 UFMT 18480-6
Pseudopaludicola saltica Brazil Mato Grosso Chapadados Guimaraes (type-locality 15∘2310158400910158401015840S 55∘5010158402410158401015840W)-MUFMT 482 UFMT 819 UFMT 821 UFMT 823 UFMT 1433-5 UFMT 1437-41 UFMT 2873 UFMT 2877 UFMT 2880-1F UFMT 1442 Cuiaba M UFMT 270 UFMT 473 UFMT476 UFMT 13657-68 F UFMT 13655-6) Nova Lacerda (MUFMT 13499-501) Porto Estrela Estacao Ecologica da Serradas Araras (M UFMT 561) and Vila Bela da SantıssimaTrindade (M UFMT 4082 UFMT 4112 UFMT 4123 UFMT4147 UFMT4153 UFMT4157 UFMT4172)MatoGrosso doSul Sonora (M UFMT 1147 UFMT 1195)
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho (type-locality 20∘0610158403210158401015840S 43∘5810158405310158401015840W)-F MCNAM 3675 MUFMT 18424 UFMT 18451 MCNAM 3677-8 MCNAM3680 Itabirito (20∘1310158402910158401015840S 43∘4810158404910158401015840W)-F MCNAM14620-1 M MCNAM 14625 Lavras Novas (20∘2810158405710158401015840S43∘3010158405210158401015840W)-F MCNAM 3694 M MCNAM 3695MCNAM 3690 Mariana (20∘0910158401210158401015840S 43∘3010158400210158401015840W)-FMCNAM 6465 M MCNAM 6457 MCNAM 6461-2 OuroBranco (20∘3010158401610158401015840S 43∘4210158400410158401015840W)-M MCNAM 6559 SaoJoao Del Rei (21∘0810158402510158401015840S 44∘1710158403110158401015840W)-M UFMT 18425-6UFMT 18452-3 and Botumirim (16∘4410158401310158401015840S 42∘3410158402910158401015840W)-FMCNAM 6713 M MCNAM 6832 MCNAM 6834 MCNAM6636 MCNAM 6642-3
B Analyzed Sound Files
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality) LH 676 no voucher specimen LH 677 call
fromUFMT 18455 LH 678 call fromUFMT 18395 and FNJV12976 no voucher specimen Minas Gerais Sao Roque deMinas (20∘1310158402010158401015840S 46∘2710158402410158401015840W) FNJV 4575 no voucherspecimen and Pocos de Caldas (21∘5510158400410158401015840S 46∘3410158400210158401015840W)FNJV 4576 no voucher specimen
Pseudopaludicola mystacalis Brazil Ceara Itapipoca(03∘2410158405810158401015840S 39∘4110158403110158401015840W) LH 655 no voucher specimenTaiba (03∘2510158404410158401015840S 38∘5710158404310158401015840W) LH 658 no voucher spec-imen Goias Uruacu LH 639 call from UFMT 18410) MatoGrosso Chapada dos Guimaraes (type-locality) LH 13A-05no voucher specimen) Caceres LH 47A-04 call fromUFMT10451 Cuiaba LH 14A-01 call from UFMT 2426 LH 14A-02 call from UFMT 2424 Pocone LH 01A-01 call fromUFMT 4321 and Nossa Senhora do Livramento LH 04A-10 call from UFMT 4330 Maranhao Balsa (07∘2810158404910158401015840S46∘0310158401910158401015840W) LH 284 no voucher specimen Piauı Brejo doPiauı (08∘1110158405010158401015840S 42∘4910158405910158401015840W) LH 184 call from UFMT11202 Para Primavera LH 352 call from UFMT 11836 SaoPaulo Icem LH 701 call from UFMT 18423
Pseudopaludicola saltica BrazilMatoGrossoCuiaba LH13A-01 call fromUFMT 8187Nova Lacerda LH 42A-06 callfrom UFMT 13499 LH 42A-07 call from UFMT 13500 andPorto Estrela LH 12 no voucher specimen LH 13 call fromUFMT 13678 LH 14 call fromUFMT 16423 LH 16 call fromUFMT 16417 LH 17 call from UFMT 16414 and LH 18 callfrom UFMT 16385 Minas Gerais Uberlandia (18∘5810158403010158401015840S48∘1710158402610158401015840W) LH 709 no voucher specimen
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho LH 673call from UFMT 18451 LH 674 no voucher specimen andSao Joao Del Rei LH 675 call from UFMT 18426 and FNJV12879-80 no voucher specimen
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Special thanks go to Felipe Franco Curcio Diva MariaBorges-Nojosa and Luciana Barreto Nascimento for allow-ing access to the material under their care at ldquoColecaoZoologica de Vertebrados da Universidade Federal de MatoGrossordquo (UFMT) ldquoColecao Herpetologica da UniversidadeFederal do Cearardquo (UFC) and ldquoMuseu de Ciencias Naturaisrdquo(MCNAM Belo Horizonte Minas Gerais) respectively toAdao J Cardoso (in memoriam) and Luis F Toledo for therecordings and for allowing access respectively to bioa-coustic samples deposited at ldquoFonoteca Neotropical JacquesVielliardrdquo (FNJV) to the CNPq project ldquoRede de pesquisa emanfıbios e repteis de ecossistemas nao florestais brasileirosrdquo(Process no 5633522010-8) for logistical support to VivianUhlig (RANICMBio) for estimates of extent of occurrenceAndre Pansonato thanks ldquoCoordenacao de Aperfeicoamentode Pessoal de Nivel Superiorrdquo (CAPES) for a PhD scholar-ship and Christine Strussmann thanks CNPq for a researchfellowship (Process no 3095412012-3)
Advances in Zoology 13
References
[1] K D Wells The Ecology amp Behavior of Amphibians TheUniversity of Chicago Chicago Ill USA 2007
[2] M Vences M Gehara J Kohler and F Glaw ldquoDescription of anewMalagasy treefrog (Boophis) occurring syntopically with itssister species and a plea for studies on non-allopatric speciationin tropical amphibiansrdquo Amphibia Reptilia vol 33 no 3-4 pp503ndash520 2012
[3] I De La Riva R Marquez and J Bosch ldquoDescription ofthe advertisement calls of some South American Hylidae(Amphibia Anura) taxonomic and methodological conse-quencesrdquo Bonner Zoologische Beitrage vol 47 pp 175ndash185 1997
[4] F S de Andrade and T R de Carvalho ldquoA new species of Pseu-dopaludicola Miranda-Ribeiro (Leiuperinae LeptodactylidaeAnura) from the Cerrado of southeastern Brazilrdquo Zootaxa vol3608 no 5 pp 389ndash397 2013
[5] D Cardozo and L F Toledo ldquoTaxonomic status of Pseudopalu-dicola riopiedadensis Mercadal de Barrio and Barrio 1994(Anura Leptodactylidae Leiuperinae)rdquo Zootaxa vol 3734 pp571ndash582 2013
[6] T R de Carvalho ldquoA new species of PseudopaludicolaMiranda-Ribeiro (Leiuperinae Leptodactylidae Anura) from the Cer-rado of southeastern Brazil with a distinctive advertisement callpatternrdquo Zootaxa no 3328 pp 47ndash54 2012
[7] F M Magalhaes D Loebmann M N C Kokubum C F BHaddad and A A Garda ldquoA new species of Pseudopaludi-cola (Anura Leptodactylidae Leiuperinae) from NortheasternBrazilrdquo Herpetologica vol 70 pp 77ndash88 2014
[8] A Pansonato C Strussmann J R Mudrek and I A Mar-tins ldquoMorphometric and bioacoustic data on three species ofPseudopaludicola Miranda-Ribeiro 1926 (Anura Leptodactyl-idae Leiuperinae) described from Chapada dos GuimaraesMato Grosso Brazil with the revalidation of Pseudopaludicolaameghini (Cope 1887)rdquo Zootaxa vol 3620 no 1 pp 147ndash1622013
[9] I J Roberto D Cardozo and R W Avila ldquoA new speciesof Pseudopaludicola (Anura Leiuperidae) from Western PiauıState Northeast Brazilrdquo Zootaxa vol 3636 no 2 pp 348ndash3602013
[10] S B Barreto M S Tinoco D Couto-Ferreira and H CBrowne-Ribeiro ldquoDistribuicao de Pseudopaludicola aff falcipes(Anura Leiuperidae) na restinga do litoral norte da BahiaBrasilrdquoRevista Latino-Americana de Conservacao vol 2 pp 27ndash36 2012
[11] E R Favero A C P Veiga-Menoncello D C Rossa-Feres et alldquoIntrageneric karyotypic variation in Pseudopaludicola (AnuraLeiuperidae) and its taxonomic relatednessrdquo Zoological Studiesvol 50 no 6 pp 826ndash836 2011
[12] M Jansen R Bloch A Schulze andM Pfenninger ldquoIntegrativeinventory of Boliviarsquos lowland anurans reveals hidden diversityrdquoZoologica Scripta vol 40 no 6 pp 567ndash583 2011
[13] C P D Prado M Uetanabaro and C F B Haddad ldquoBreed-ing activity patterns reproductive modes and habitat use byanurans (Amphibia) in a seasonal environment in the PantanalBrazilrdquo Amphibia Reptilia vol 26 no 2 pp 211ndash221 2005
[14] R A Silva I A Martins and D C Rossa-Feres ldquoBioacustica esıtio de vocalizacao em taxocenoses de anfıbios de area abertano Noroeste Paulistardquo Biota Neotropica vol 8 pp 123ndash1342008
[15] L F Toledo ldquoDescription of a new species of PseudopaludicolaMiranda-Ribeiro 1926 from the state of Sao Paulo SoutheasternBrazil (Anura Leiuperidae)rdquoZootaxa no 2681 pp 47ndash56 2010
[16] L F Toledo S Siqueira T CDuarte A C P Veiga-MenoncelloS M Recco-Pimentel and C F B Haddad ldquoDescription of anew species of Pseudopaludicola Miranda-Ribeiro 1926 fromthe state of Sao Paulo Southeastern Brazil (Anura Leiuperi-dae)rdquo Zootaxa no 2496 pp 38ndash48 2010
[17] C F B Haddad and A J Cardoso ldquoTaxonomia de tres especiesde Pseudopaludicola (Anura Leptodactylidae)rdquo Papeis Avulsosde Zoologia vol 36 pp 287ndash300 1987
[18] T C Duarte A C P Veiga-Menoncello J F R Lima et alldquoChromosome analysis in Pseudopaludicola (Anura Leiuperi-dae) with description of sex chromosomes XXXY in P salticardquoHereditas vol 147 no 2 pp 43ndash52 2010
[19] A C P Veiga-Menoncello L B Lourenco C Strussmannet al ldquoA phylogenetic analysis of Pseudopaludicola (Anura)providing evidence of progressive chromosome reductionrdquoZoologica Scripta vol 43 no 3 pp 261ndash272 2014
[20] W R Heyer A S Rand C A G Cruz O L Peixoto and CE Nelson ldquoFrogs of Boraceiardquo Arquivos de Zoologia vol 31 pp231ndash410 1990
[21] W E Duellman The Hylid Frogs of Middle America vol 1 ofMonograph of the Museum of Natural History of University ofKansas 1970
[22] R Development Core Team The R Project for Statistical Com-puting Vienna Austria 2013 httpwwwr-projectorg
[23] P E Vanzolini ldquoEcological and geographical distribution oflizards in Pernambuco Northeastern Brasil (Sauria)rdquo PapeisAvulsos de Zoologia vol 18 no 4 pp 61ndash90 1974
[24] J M Cei ldquoAmphibians of Argentinardquo Monitore ZoologicoItaliano Nuova Serie Monografia vol 2 pp 1ndash609 1980
[25] F Brusquetti and E O Lavilla ldquoLista comentada de los anfibiosde ParaguayrdquoCuadernos deHerpetologıa vol 20 no 2 pp 3ndash792006
[26] I De La Riva J Kohler S Lotters and S Reichle ldquoTenyears of research on Bolivian amphibians updated checklistdistribution taxonomic problems literature and iconographyrdquoRevista Espanola Herpetologica vol 14 pp 19ndash164 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
8 Advances in Zoology
3
2
1
0
minus1
minus2
210minus1minus2minus3
DF2
(37
)
DF1 (63)
(a)
3
2
1
0
minus1
minus2
minus3
3210minus1minus2minus3minus4
DF2
(15
)
DF1 (85)
(b)
2
1
0
minus1
210minus1minus2
DF1 (79)
DF2
(21
)
Chapada dos Guimaraes-MTCuiab a-MTNS Livramento-MTPorto Estrela-MTC aceres-MTBarra do Garccedilas-MTPocon e-MTUruaccedilu-GO
Alto Alegre-SP
Primavera-PAItapipoca-CETaBalsas-MABrejo do Piauı-PIacute
ıba-CE
Ic em-SP
(c)
Figure 3 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of 101 males (a) 37 females (b)and six bioacoustic variables (c) of Pseudopaludicola mystacalis from 15 different localities in Brazil
Maximum variation in temporal variables (notes perminute and number of pulses) of the calls of all specimensanalyzed is 2136 notesmin and 8 pulsesnote In the mostdistant known locations the difference in the number of notesper minute and in the number of pulses is 1003 notesmin
and 6 pulsesnote respectively Considering subsets of pop-ulations from Brazilian Northeast and Brazilian Midwestmaximum interpopulational variation is 1146 notesmin and1335 notesmin respectively There are 7 pulsesnote in callsfrom populations of both areas Maximum intrapopulational
Advances in Zoology 9
Pseudopaludicola serrana Pseudopaludicola murundu Pseudopaludicola saltica
05 1 15 2 25 3 35 4 45 5
A B C D E F G H I(k
Hz)
8
7
6
5
4
3
2
1
(s)
Figure 4 Spectrograms (DFT size = 512 samples two notes for each locality) of advertisement calls of Pseudopaludicola serrana (AndashC) andP murundu (DndashF) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais-Uberlandia (G) state of MatoGrosso-Chapada dos Guimaraes (type-locality H) and Porto Estrela (I)
Note Pulses
(a) (b)
(c) (d)
(e) (f)
(g) (h)
Figure 5 Oscillograms of advertisement calls of Pseudopaludicola serrana (a)-(b) and P murundu (c)ndash(e) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais Uberlandia (f) state of Mato Grosso Chapada dos Guimaraes (type-locality (g))and Porto Estrela (h) Total time of each oscillogram corresponds to 05 s
10 Advances in Zoology
4
2
0
minus2
minus4
6420minus2minus4
DF2
(2
)
DF1 (98)
(a)
4
2
0
minus2
minus4
6420minus2minus4
DF2
(1
)
DF1 (99)
(b)
Figure 6 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of males (a) and six bioacousticvariables (b) of Pseudopaludicola murundu (open circles) P saltica (triangles) and P serrana (closed circles)
Elevation (m)
0
(km)
minus155ndash350351ndash700701ndash1050
1050ndash14001401ndash1750
300
N
1
2
3
4
5
6 78
91011
12
13
Figure 7 Geographical distribution of Pseudopaludicola murundu(circles) and P saltica (triangles) in southeastern Brazil state of SaoPaulomdashRioClaro (type locality (1)) andCampinas (2) state ofMinasGeraismdashPocos de Caldas (3) Alpinopolis (4) (see [17]) Sao Roquede Minas (5) Sao Joao Del Rei (6) Mariana (7) Ouro Branco (8)Itabirito (9) Brumadinho (10) Lavras Novas (11) Botumirim (12)and Uberlandia (13)
variation in the number of notes per minute and in thenumber of pulses in four localities from the state of MatoGrosso is 81 notesmin in Cuiaba and 5 pulsesnote in Cuiabaand Nossa Senhora do Livramento (see Table 3 and [8])Mean note duration does not differ significantly in all theexamined calls (Table 3 119865 = 49 df = 2 119875 = 003)
Table 5 Summary of the number of male specimens correctlyclassified as Pseudopaludicolamurundu P saltica or P serrana usingdiscriminant function analysis of 12 morphometric measurementsand seven bioacoustic variables
Morphometric measurementsTrue group
P murundu P saltica P serranaP murundu 1 0 5P saltica 0 39 0P serrana 3 0 19Total number 6 39 22 16 100 86
Bioacoustic variablesTrue group
P murundu P saltica P serranaP murundu 5 0 1P saltica 0 8 1P serrana 3 0 2Total number 6 9 5 83 889 40
Acoustic analysis of geographical variation in specieswith an extent of occurrence of the magnitude seen inP mystacalis sometimes reveals cryptic taxa being treatedunder a single name However this was not the case in Pmystacalis a taxon that remained erroneously characterizedand poorly recognized in the literature until recently [8] Ourresults reveal a relatively small variation in morphologicaland acoustical traits of P mystacalis and allow confirming thepresence of the species in a wide geographical area along theBrazilian open ecosystems
Advances in Zoology 11
Table 6 Ratios of selected measurements (in mm) of males of Pseudopaludicola murundu P salticaand P serrana Values are presented asmean plusmn standard deviation119873 = number of specimens analyzed
HLSVL HWSVL HLHW HALSVL FLSVL THLSVL TLSVLP serrana (119873 = 21) 040 plusmn 003 036 plusmn 002 110 plusmn 006 027 plusmn 002 061 plusmn 004 056 plusmn 003 070 plusmn 003
P murundu (119873 = 5) 039 plusmn 004 035 plusmn 003 111 plusmn 009 027 plusmn 001 066 plusmn 002 056 plusmn 002 070 plusmn 003
P saltica (119873 = 44) 041 plusmn 004 038 plusmn 003 109 plusmn 011 026 plusmn 003 068 plusmn 006 055 plusmn 005 073 plusmn 005
HAL hand length HL head length HW head width FL foot length SVL snout-vent length THL thigh length TL tibia length
42 Taxonomic Status of Pseudopaludicola serrana Toledo2010 When describing P serrana Toledo [15] used asmorphological characteristics separating the three speciesbelonging to the P saltica group the aspect (relative size andcoloration) of nuptial pads in the external part of finger I andaspect of the vocal sac Such characteristics allow differingP serrana and P murundu from P saltica but do not allowdiffering P serrana from P murundu [15] Previously Haddadand Cardoso [17] had called attention to the fact that nuptialpads were more developed in specimens of P saltica from thetype-locality (Chapada do Guimaraes Mato Grosso) than inspecimens collected and recorded in localities in the statesof Minas Gerais and Sao Paulo In the same article Haddadand Cardoso [17] also presented a spectrogram of the callof a specimen from Campinas Sao Paulo Based on suchreported morphological evidence and acoustic parameterswe here argue that specimens from Minas Gerais and SaoPaulo attributed to P saltica in Haddad and Cardoso [17] infact correspond to P murundu
The only external morphological characteristic used byToledo [15] to differ P serrana from P murunduwas a shorterhead lengthheadwidth ratio (HLHW= 097plusmn006 in the fiveindividuals ofP serrana evaluated 111plusmn007 in 11 individualsof P murundu) After having analyzed a higher number ofspecimens attributed to P serrana (119873 = 21) we found thatHLHW (110 plusmn 006 see Table 6) in this sample does notdiffer from the values presented in the original descriptionand confirmed herein for P murundu
The description of P serrana was also based on physicalcharacteristics of its advertisement calls [15] However theoriginal dataset is relatively low 12 notes of a single maleof P saltica 14 notes of 2 males of P murundu and 15notes of 3 males of P serrana were analyzed and comparedOnly one out of four acoustic variables (pulse duration) wasconsidered diagnostic for the new species Toledo [15] alsoshowed that dominant frequency range of P serrana wascompletely nested within the dominant frequency range of Pmurundu However when later proposing the synonymiza-tion of Pseudopaludicola riopiedadensis Mercadal de Bar-rio and Barrio 1994 to Pseudopaludicola ternetzi Miranda-Ribeiro 1937 Cardozo and Toledo [5] based their decision onldquoseveral important overlapsrdquo including dominant frequencyranges between the two species Indeed our data showedthat dominant frequency contributed to higher loadingsto separate species in the P saltica group Nonoverlappingdominant frequencies would therefore be expected betweenrelated but distinct species of Pseudopaludicola
Bioacoustic data have proven to be useful for uncoveringmorphologically cryptic species in the genus Pseudopaludi-cola [4ndash9 15 16] Advertisement calls of species in this genusmight be divided into three distinct groups according to typeof notes nonpulsed notes notes with concatenated pulsesand noteswith nonconcatenated pulses [7] Each groupmightbe diagnosed by temporal (pulses per note note and pulseduration internotes and interpulses intervals note rate andpulse rate) and spectral variables (dominant frequency andharmonics) which in combination allow characterizing allthe species for which calls were already analyzed except forP serrana and P murundu As evidenced by the recent syn-onymization of Pseudopaludicola riopiedadensis to P ternetzi[15] and reinforced herein by the proposed synonymizationof P serrana to P murundu morphologically similar speciesof Pseudopaludicola presenting the same type of note and anoverlap in their spectral acoustic variables are expected torepresent the same taxon Therefore no arguments remainto consider P serrana as a distinct species from P murunduand the former must be considered as a junior synonym of Pmurundu
5 Conclusions
We here report on the variation in morphometric charactersand variation in bioacoustic variables of the advertisementcalls in fifteen Brazilian populations of Pseudopaludicolamys-tacalis Although limited our sample evidenced no statisticaldifferences in any of the evaluated attributes and allowed usto confirm that this species is widely distributed in BrazilMorphometric and bioacoustic data did not differ also inpopulations currently attributed to Pseudopaludicola serranaand Pseudopaludicola murundu and the former taxon ishere considered as a junior synonym of P murundu Thedata in the present work aims at contributing to a betterunderstanding of the diversity and distribution patterns inthe genus Pseudopaludicola
Appendices
A Voucher Specimens Examined
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality 22∘1910158405210158401015840S 47∘4210158405610158401015840W)-F UFMT 18454MUFMT 18395-6 UFMT 18455-7
Pseudopaludicola mystacalis Brazil Para Primavera(00∘5710158402210158401015840S 47∘0710158401210158401015840W)-M UFMT 11651 UFMT 11827
12 Advances in Zoology
UFMT 11833 UFMT 11836 UFMT 11839 Goias Uruacu(14∘3110158403510158401015840S 49∘0710158405410158401015840W)-F UFMT 18397-400 UFMT18458-9 M UFMT 18401-15 UFMT 18458-64 Mato GrossoBarra do Garcas (15∘3110158405710158401015840S 52∘1410158401010158401015840W)-M UFMT11097 UFMT 11307 UFMT 11319 UFMT 11324 Caceres(16∘1710158405910158401015840S 58∘0910158400910158401015840W)-F UFMT 5906 UFMT 5950UFMT 5955 UFMT 5962 UFMT 9152 UFMT 10445UFMT 10448 UFMT 13669 M UFMT 10451-2 UFMT10455 UFMT 10458 UFMT 10466 UFMT 10495 UFMT10506 UFMT 10508 UFMT 13670 Chapada dos Guimaraes(type-locality 14∘5010158403410158401015840S 55∘2310158401010158401015840W)-F UFMT 8109 MUFMT 487 UFMT 817 UFMT 820 UFMT 12890 Cuiaba(15∘3910158403310158401015840S 55∘5610158403010158401015840W)-M UFMT 15980 UFMT 2426UFMT 2430 UFMT 2432 UFMT 2434-7 UFMT 2439UFMT 7399 UFMT 7653 UFMT 8177-8 UFMT 8180UFMT 8182 UFMT 8184-5 UFMT 13671 Nossa Senhorado Livramento (16∘2110158405810158401015840S 56∘1810158403310158401015840W)-F UFMT 18465UFMT 352 UFMT 6436 UFMT 6466-7 UFMT 6488UFMT 6511 M UFMT 4343 UFMT 6487 UFMT 6491UFMT6498UFMT6515Pocone (16∘3010158405810158401015840S 56∘4410158405310158401015840W)-M UFMT 348-50 UFMT 889 UFMT 4316 UFMT 4318UFMT 4321 UFMT 13672 and Porto Estrela (15∘3510158400510158401015840S57∘1310158402010158401015840W)-F UFMT 18466-7 UFMT 138 UFMT 13482M UFMT 18468-9 UFMT 402 UFMT 2200 UFMT 11346Sao Paulo Icem (20∘2010158403110158401015840S 49∘1110158404210158401015840W)-F UFMT 18421UFMT 18470-2 M UFMT 18422-3 UFMT 18473 and AltoAlegre (21∘3310158402010158401015840S 50∘1310158402210158401015840W)-F UFMT 18474-5 UFMT18479 MUFMT 18476-8 UFMT 18480-6
Pseudopaludicola saltica Brazil Mato Grosso Chapadados Guimaraes (type-locality 15∘2310158400910158401015840S 55∘5010158402410158401015840W)-MUFMT 482 UFMT 819 UFMT 821 UFMT 823 UFMT 1433-5 UFMT 1437-41 UFMT 2873 UFMT 2877 UFMT 2880-1F UFMT 1442 Cuiaba M UFMT 270 UFMT 473 UFMT476 UFMT 13657-68 F UFMT 13655-6) Nova Lacerda (MUFMT 13499-501) Porto Estrela Estacao Ecologica da Serradas Araras (M UFMT 561) and Vila Bela da SantıssimaTrindade (M UFMT 4082 UFMT 4112 UFMT 4123 UFMT4147 UFMT4153 UFMT4157 UFMT4172)MatoGrosso doSul Sonora (M UFMT 1147 UFMT 1195)
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho (type-locality 20∘0610158403210158401015840S 43∘5810158405310158401015840W)-F MCNAM 3675 MUFMT 18424 UFMT 18451 MCNAM 3677-8 MCNAM3680 Itabirito (20∘1310158402910158401015840S 43∘4810158404910158401015840W)-F MCNAM14620-1 M MCNAM 14625 Lavras Novas (20∘2810158405710158401015840S43∘3010158405210158401015840W)-F MCNAM 3694 M MCNAM 3695MCNAM 3690 Mariana (20∘0910158401210158401015840S 43∘3010158400210158401015840W)-FMCNAM 6465 M MCNAM 6457 MCNAM 6461-2 OuroBranco (20∘3010158401610158401015840S 43∘4210158400410158401015840W)-M MCNAM 6559 SaoJoao Del Rei (21∘0810158402510158401015840S 44∘1710158403110158401015840W)-M UFMT 18425-6UFMT 18452-3 and Botumirim (16∘4410158401310158401015840S 42∘3410158402910158401015840W)-FMCNAM 6713 M MCNAM 6832 MCNAM 6834 MCNAM6636 MCNAM 6642-3
B Analyzed Sound Files
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality) LH 676 no voucher specimen LH 677 call
fromUFMT 18455 LH 678 call fromUFMT 18395 and FNJV12976 no voucher specimen Minas Gerais Sao Roque deMinas (20∘1310158402010158401015840S 46∘2710158402410158401015840W) FNJV 4575 no voucherspecimen and Pocos de Caldas (21∘5510158400410158401015840S 46∘3410158400210158401015840W)FNJV 4576 no voucher specimen
Pseudopaludicola mystacalis Brazil Ceara Itapipoca(03∘2410158405810158401015840S 39∘4110158403110158401015840W) LH 655 no voucher specimenTaiba (03∘2510158404410158401015840S 38∘5710158404310158401015840W) LH 658 no voucher spec-imen Goias Uruacu LH 639 call from UFMT 18410) MatoGrosso Chapada dos Guimaraes (type-locality) LH 13A-05no voucher specimen) Caceres LH 47A-04 call fromUFMT10451 Cuiaba LH 14A-01 call from UFMT 2426 LH 14A-02 call from UFMT 2424 Pocone LH 01A-01 call fromUFMT 4321 and Nossa Senhora do Livramento LH 04A-10 call from UFMT 4330 Maranhao Balsa (07∘2810158404910158401015840S46∘0310158401910158401015840W) LH 284 no voucher specimen Piauı Brejo doPiauı (08∘1110158405010158401015840S 42∘4910158405910158401015840W) LH 184 call from UFMT11202 Para Primavera LH 352 call from UFMT 11836 SaoPaulo Icem LH 701 call from UFMT 18423
Pseudopaludicola saltica BrazilMatoGrossoCuiaba LH13A-01 call fromUFMT 8187Nova Lacerda LH 42A-06 callfrom UFMT 13499 LH 42A-07 call from UFMT 13500 andPorto Estrela LH 12 no voucher specimen LH 13 call fromUFMT 13678 LH 14 call fromUFMT 16423 LH 16 call fromUFMT 16417 LH 17 call from UFMT 16414 and LH 18 callfrom UFMT 16385 Minas Gerais Uberlandia (18∘5810158403010158401015840S48∘1710158402610158401015840W) LH 709 no voucher specimen
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho LH 673call from UFMT 18451 LH 674 no voucher specimen andSao Joao Del Rei LH 675 call from UFMT 18426 and FNJV12879-80 no voucher specimen
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Special thanks go to Felipe Franco Curcio Diva MariaBorges-Nojosa and Luciana Barreto Nascimento for allow-ing access to the material under their care at ldquoColecaoZoologica de Vertebrados da Universidade Federal de MatoGrossordquo (UFMT) ldquoColecao Herpetologica da UniversidadeFederal do Cearardquo (UFC) and ldquoMuseu de Ciencias Naturaisrdquo(MCNAM Belo Horizonte Minas Gerais) respectively toAdao J Cardoso (in memoriam) and Luis F Toledo for therecordings and for allowing access respectively to bioa-coustic samples deposited at ldquoFonoteca Neotropical JacquesVielliardrdquo (FNJV) to the CNPq project ldquoRede de pesquisa emanfıbios e repteis de ecossistemas nao florestais brasileirosrdquo(Process no 5633522010-8) for logistical support to VivianUhlig (RANICMBio) for estimates of extent of occurrenceAndre Pansonato thanks ldquoCoordenacao de Aperfeicoamentode Pessoal de Nivel Superiorrdquo (CAPES) for a PhD scholar-ship and Christine Strussmann thanks CNPq for a researchfellowship (Process no 3095412012-3)
Advances in Zoology 13
References
[1] K D Wells The Ecology amp Behavior of Amphibians TheUniversity of Chicago Chicago Ill USA 2007
[2] M Vences M Gehara J Kohler and F Glaw ldquoDescription of anewMalagasy treefrog (Boophis) occurring syntopically with itssister species and a plea for studies on non-allopatric speciationin tropical amphibiansrdquo Amphibia Reptilia vol 33 no 3-4 pp503ndash520 2012
[3] I De La Riva R Marquez and J Bosch ldquoDescription ofthe advertisement calls of some South American Hylidae(Amphibia Anura) taxonomic and methodological conse-quencesrdquo Bonner Zoologische Beitrage vol 47 pp 175ndash185 1997
[4] F S de Andrade and T R de Carvalho ldquoA new species of Pseu-dopaludicola Miranda-Ribeiro (Leiuperinae LeptodactylidaeAnura) from the Cerrado of southeastern Brazilrdquo Zootaxa vol3608 no 5 pp 389ndash397 2013
[5] D Cardozo and L F Toledo ldquoTaxonomic status of Pseudopalu-dicola riopiedadensis Mercadal de Barrio and Barrio 1994(Anura Leptodactylidae Leiuperinae)rdquo Zootaxa vol 3734 pp571ndash582 2013
[6] T R de Carvalho ldquoA new species of PseudopaludicolaMiranda-Ribeiro (Leiuperinae Leptodactylidae Anura) from the Cer-rado of southeastern Brazil with a distinctive advertisement callpatternrdquo Zootaxa no 3328 pp 47ndash54 2012
[7] F M Magalhaes D Loebmann M N C Kokubum C F BHaddad and A A Garda ldquoA new species of Pseudopaludi-cola (Anura Leptodactylidae Leiuperinae) from NortheasternBrazilrdquo Herpetologica vol 70 pp 77ndash88 2014
[8] A Pansonato C Strussmann J R Mudrek and I A Mar-tins ldquoMorphometric and bioacoustic data on three species ofPseudopaludicola Miranda-Ribeiro 1926 (Anura Leptodactyl-idae Leiuperinae) described from Chapada dos GuimaraesMato Grosso Brazil with the revalidation of Pseudopaludicolaameghini (Cope 1887)rdquo Zootaxa vol 3620 no 1 pp 147ndash1622013
[9] I J Roberto D Cardozo and R W Avila ldquoA new speciesof Pseudopaludicola (Anura Leiuperidae) from Western PiauıState Northeast Brazilrdquo Zootaxa vol 3636 no 2 pp 348ndash3602013
[10] S B Barreto M S Tinoco D Couto-Ferreira and H CBrowne-Ribeiro ldquoDistribuicao de Pseudopaludicola aff falcipes(Anura Leiuperidae) na restinga do litoral norte da BahiaBrasilrdquoRevista Latino-Americana de Conservacao vol 2 pp 27ndash36 2012
[11] E R Favero A C P Veiga-Menoncello D C Rossa-Feres et alldquoIntrageneric karyotypic variation in Pseudopaludicola (AnuraLeiuperidae) and its taxonomic relatednessrdquo Zoological Studiesvol 50 no 6 pp 826ndash836 2011
[12] M Jansen R Bloch A Schulze andM Pfenninger ldquoIntegrativeinventory of Boliviarsquos lowland anurans reveals hidden diversityrdquoZoologica Scripta vol 40 no 6 pp 567ndash583 2011
[13] C P D Prado M Uetanabaro and C F B Haddad ldquoBreed-ing activity patterns reproductive modes and habitat use byanurans (Amphibia) in a seasonal environment in the PantanalBrazilrdquo Amphibia Reptilia vol 26 no 2 pp 211ndash221 2005
[14] R A Silva I A Martins and D C Rossa-Feres ldquoBioacustica esıtio de vocalizacao em taxocenoses de anfıbios de area abertano Noroeste Paulistardquo Biota Neotropica vol 8 pp 123ndash1342008
[15] L F Toledo ldquoDescription of a new species of PseudopaludicolaMiranda-Ribeiro 1926 from the state of Sao Paulo SoutheasternBrazil (Anura Leiuperidae)rdquoZootaxa no 2681 pp 47ndash56 2010
[16] L F Toledo S Siqueira T CDuarte A C P Veiga-MenoncelloS M Recco-Pimentel and C F B Haddad ldquoDescription of anew species of Pseudopaludicola Miranda-Ribeiro 1926 fromthe state of Sao Paulo Southeastern Brazil (Anura Leiuperi-dae)rdquo Zootaxa no 2496 pp 38ndash48 2010
[17] C F B Haddad and A J Cardoso ldquoTaxonomia de tres especiesde Pseudopaludicola (Anura Leptodactylidae)rdquo Papeis Avulsosde Zoologia vol 36 pp 287ndash300 1987
[18] T C Duarte A C P Veiga-Menoncello J F R Lima et alldquoChromosome analysis in Pseudopaludicola (Anura Leiuperi-dae) with description of sex chromosomes XXXY in P salticardquoHereditas vol 147 no 2 pp 43ndash52 2010
[19] A C P Veiga-Menoncello L B Lourenco C Strussmannet al ldquoA phylogenetic analysis of Pseudopaludicola (Anura)providing evidence of progressive chromosome reductionrdquoZoologica Scripta vol 43 no 3 pp 261ndash272 2014
[20] W R Heyer A S Rand C A G Cruz O L Peixoto and CE Nelson ldquoFrogs of Boraceiardquo Arquivos de Zoologia vol 31 pp231ndash410 1990
[21] W E Duellman The Hylid Frogs of Middle America vol 1 ofMonograph of the Museum of Natural History of University ofKansas 1970
[22] R Development Core Team The R Project for Statistical Com-puting Vienna Austria 2013 httpwwwr-projectorg
[23] P E Vanzolini ldquoEcological and geographical distribution oflizards in Pernambuco Northeastern Brasil (Sauria)rdquo PapeisAvulsos de Zoologia vol 18 no 4 pp 61ndash90 1974
[24] J M Cei ldquoAmphibians of Argentinardquo Monitore ZoologicoItaliano Nuova Serie Monografia vol 2 pp 1ndash609 1980
[25] F Brusquetti and E O Lavilla ldquoLista comentada de los anfibiosde ParaguayrdquoCuadernos deHerpetologıa vol 20 no 2 pp 3ndash792006
[26] I De La Riva J Kohler S Lotters and S Reichle ldquoTenyears of research on Bolivian amphibians updated checklistdistribution taxonomic problems literature and iconographyrdquoRevista Espanola Herpetologica vol 14 pp 19ndash164 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
Advances in Zoology 9
Pseudopaludicola serrana Pseudopaludicola murundu Pseudopaludicola saltica
05 1 15 2 25 3 35 4 45 5
A B C D E F G H I(k
Hz)
8
7
6
5
4
3
2
1
(s)
Figure 4 Spectrograms (DFT size = 512 samples two notes for each locality) of advertisement calls of Pseudopaludicola serrana (AndashC) andP murundu (DndashF) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais-Uberlandia (G) state of MatoGrosso-Chapada dos Guimaraes (type-locality H) and Porto Estrela (I)
Note Pulses
(a) (b)
(c) (d)
(e) (f)
(g) (h)
Figure 5 Oscillograms of advertisement calls of Pseudopaludicola serrana (a)-(b) and P murundu (c)ndash(e) recorded at their respective type-localities and P saltica recorded in state of Minas Gerais Uberlandia (f) state of Mato Grosso Chapada dos Guimaraes (type-locality (g))and Porto Estrela (h) Total time of each oscillogram corresponds to 05 s
10 Advances in Zoology
4
2
0
minus2
minus4
6420minus2minus4
DF2
(2
)
DF1 (98)
(a)
4
2
0
minus2
minus4
6420minus2minus4
DF2
(1
)
DF1 (99)
(b)
Figure 6 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of males (a) and six bioacousticvariables (b) of Pseudopaludicola murundu (open circles) P saltica (triangles) and P serrana (closed circles)
Elevation (m)
0
(km)
minus155ndash350351ndash700701ndash1050
1050ndash14001401ndash1750
300
N
1
2
3
4
5
6 78
91011
12
13
Figure 7 Geographical distribution of Pseudopaludicola murundu(circles) and P saltica (triangles) in southeastern Brazil state of SaoPaulomdashRioClaro (type locality (1)) andCampinas (2) state ofMinasGeraismdashPocos de Caldas (3) Alpinopolis (4) (see [17]) Sao Roquede Minas (5) Sao Joao Del Rei (6) Mariana (7) Ouro Branco (8)Itabirito (9) Brumadinho (10) Lavras Novas (11) Botumirim (12)and Uberlandia (13)
variation in the number of notes per minute and in thenumber of pulses in four localities from the state of MatoGrosso is 81 notesmin in Cuiaba and 5 pulsesnote in Cuiabaand Nossa Senhora do Livramento (see Table 3 and [8])Mean note duration does not differ significantly in all theexamined calls (Table 3 119865 = 49 df = 2 119875 = 003)
Table 5 Summary of the number of male specimens correctlyclassified as Pseudopaludicolamurundu P saltica or P serrana usingdiscriminant function analysis of 12 morphometric measurementsand seven bioacoustic variables
Morphometric measurementsTrue group
P murundu P saltica P serranaP murundu 1 0 5P saltica 0 39 0P serrana 3 0 19Total number 6 39 22 16 100 86
Bioacoustic variablesTrue group
P murundu P saltica P serranaP murundu 5 0 1P saltica 0 8 1P serrana 3 0 2Total number 6 9 5 83 889 40
Acoustic analysis of geographical variation in specieswith an extent of occurrence of the magnitude seen inP mystacalis sometimes reveals cryptic taxa being treatedunder a single name However this was not the case in Pmystacalis a taxon that remained erroneously characterizedand poorly recognized in the literature until recently [8] Ourresults reveal a relatively small variation in morphologicaland acoustical traits of P mystacalis and allow confirming thepresence of the species in a wide geographical area along theBrazilian open ecosystems
Advances in Zoology 11
Table 6 Ratios of selected measurements (in mm) of males of Pseudopaludicola murundu P salticaand P serrana Values are presented asmean plusmn standard deviation119873 = number of specimens analyzed
HLSVL HWSVL HLHW HALSVL FLSVL THLSVL TLSVLP serrana (119873 = 21) 040 plusmn 003 036 plusmn 002 110 plusmn 006 027 plusmn 002 061 plusmn 004 056 plusmn 003 070 plusmn 003
P murundu (119873 = 5) 039 plusmn 004 035 plusmn 003 111 plusmn 009 027 plusmn 001 066 plusmn 002 056 plusmn 002 070 plusmn 003
P saltica (119873 = 44) 041 plusmn 004 038 plusmn 003 109 plusmn 011 026 plusmn 003 068 plusmn 006 055 plusmn 005 073 plusmn 005
HAL hand length HL head length HW head width FL foot length SVL snout-vent length THL thigh length TL tibia length
42 Taxonomic Status of Pseudopaludicola serrana Toledo2010 When describing P serrana Toledo [15] used asmorphological characteristics separating the three speciesbelonging to the P saltica group the aspect (relative size andcoloration) of nuptial pads in the external part of finger I andaspect of the vocal sac Such characteristics allow differingP serrana and P murundu from P saltica but do not allowdiffering P serrana from P murundu [15] Previously Haddadand Cardoso [17] had called attention to the fact that nuptialpads were more developed in specimens of P saltica from thetype-locality (Chapada do Guimaraes Mato Grosso) than inspecimens collected and recorded in localities in the statesof Minas Gerais and Sao Paulo In the same article Haddadand Cardoso [17] also presented a spectrogram of the callof a specimen from Campinas Sao Paulo Based on suchreported morphological evidence and acoustic parameterswe here argue that specimens from Minas Gerais and SaoPaulo attributed to P saltica in Haddad and Cardoso [17] infact correspond to P murundu
The only external morphological characteristic used byToledo [15] to differ P serrana from P murunduwas a shorterhead lengthheadwidth ratio (HLHW= 097plusmn006 in the fiveindividuals ofP serrana evaluated 111plusmn007 in 11 individualsof P murundu) After having analyzed a higher number ofspecimens attributed to P serrana (119873 = 21) we found thatHLHW (110 plusmn 006 see Table 6) in this sample does notdiffer from the values presented in the original descriptionand confirmed herein for P murundu
The description of P serrana was also based on physicalcharacteristics of its advertisement calls [15] However theoriginal dataset is relatively low 12 notes of a single maleof P saltica 14 notes of 2 males of P murundu and 15notes of 3 males of P serrana were analyzed and comparedOnly one out of four acoustic variables (pulse duration) wasconsidered diagnostic for the new species Toledo [15] alsoshowed that dominant frequency range of P serrana wascompletely nested within the dominant frequency range of Pmurundu However when later proposing the synonymiza-tion of Pseudopaludicola riopiedadensis Mercadal de Bar-rio and Barrio 1994 to Pseudopaludicola ternetzi Miranda-Ribeiro 1937 Cardozo and Toledo [5] based their decision onldquoseveral important overlapsrdquo including dominant frequencyranges between the two species Indeed our data showedthat dominant frequency contributed to higher loadingsto separate species in the P saltica group Nonoverlappingdominant frequencies would therefore be expected betweenrelated but distinct species of Pseudopaludicola
Bioacoustic data have proven to be useful for uncoveringmorphologically cryptic species in the genus Pseudopaludi-cola [4ndash9 15 16] Advertisement calls of species in this genusmight be divided into three distinct groups according to typeof notes nonpulsed notes notes with concatenated pulsesand noteswith nonconcatenated pulses [7] Each groupmightbe diagnosed by temporal (pulses per note note and pulseduration internotes and interpulses intervals note rate andpulse rate) and spectral variables (dominant frequency andharmonics) which in combination allow characterizing allthe species for which calls were already analyzed except forP serrana and P murundu As evidenced by the recent syn-onymization of Pseudopaludicola riopiedadensis to P ternetzi[15] and reinforced herein by the proposed synonymizationof P serrana to P murundu morphologically similar speciesof Pseudopaludicola presenting the same type of note and anoverlap in their spectral acoustic variables are expected torepresent the same taxon Therefore no arguments remainto consider P serrana as a distinct species from P murunduand the former must be considered as a junior synonym of Pmurundu
5 Conclusions
We here report on the variation in morphometric charactersand variation in bioacoustic variables of the advertisementcalls in fifteen Brazilian populations of Pseudopaludicolamys-tacalis Although limited our sample evidenced no statisticaldifferences in any of the evaluated attributes and allowed usto confirm that this species is widely distributed in BrazilMorphometric and bioacoustic data did not differ also inpopulations currently attributed to Pseudopaludicola serranaand Pseudopaludicola murundu and the former taxon ishere considered as a junior synonym of P murundu Thedata in the present work aims at contributing to a betterunderstanding of the diversity and distribution patterns inthe genus Pseudopaludicola
Appendices
A Voucher Specimens Examined
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality 22∘1910158405210158401015840S 47∘4210158405610158401015840W)-F UFMT 18454MUFMT 18395-6 UFMT 18455-7
Pseudopaludicola mystacalis Brazil Para Primavera(00∘5710158402210158401015840S 47∘0710158401210158401015840W)-M UFMT 11651 UFMT 11827
12 Advances in Zoology
UFMT 11833 UFMT 11836 UFMT 11839 Goias Uruacu(14∘3110158403510158401015840S 49∘0710158405410158401015840W)-F UFMT 18397-400 UFMT18458-9 M UFMT 18401-15 UFMT 18458-64 Mato GrossoBarra do Garcas (15∘3110158405710158401015840S 52∘1410158401010158401015840W)-M UFMT11097 UFMT 11307 UFMT 11319 UFMT 11324 Caceres(16∘1710158405910158401015840S 58∘0910158400910158401015840W)-F UFMT 5906 UFMT 5950UFMT 5955 UFMT 5962 UFMT 9152 UFMT 10445UFMT 10448 UFMT 13669 M UFMT 10451-2 UFMT10455 UFMT 10458 UFMT 10466 UFMT 10495 UFMT10506 UFMT 10508 UFMT 13670 Chapada dos Guimaraes(type-locality 14∘5010158403410158401015840S 55∘2310158401010158401015840W)-F UFMT 8109 MUFMT 487 UFMT 817 UFMT 820 UFMT 12890 Cuiaba(15∘3910158403310158401015840S 55∘5610158403010158401015840W)-M UFMT 15980 UFMT 2426UFMT 2430 UFMT 2432 UFMT 2434-7 UFMT 2439UFMT 7399 UFMT 7653 UFMT 8177-8 UFMT 8180UFMT 8182 UFMT 8184-5 UFMT 13671 Nossa Senhorado Livramento (16∘2110158405810158401015840S 56∘1810158403310158401015840W)-F UFMT 18465UFMT 352 UFMT 6436 UFMT 6466-7 UFMT 6488UFMT 6511 M UFMT 4343 UFMT 6487 UFMT 6491UFMT6498UFMT6515Pocone (16∘3010158405810158401015840S 56∘4410158405310158401015840W)-M UFMT 348-50 UFMT 889 UFMT 4316 UFMT 4318UFMT 4321 UFMT 13672 and Porto Estrela (15∘3510158400510158401015840S57∘1310158402010158401015840W)-F UFMT 18466-7 UFMT 138 UFMT 13482M UFMT 18468-9 UFMT 402 UFMT 2200 UFMT 11346Sao Paulo Icem (20∘2010158403110158401015840S 49∘1110158404210158401015840W)-F UFMT 18421UFMT 18470-2 M UFMT 18422-3 UFMT 18473 and AltoAlegre (21∘3310158402010158401015840S 50∘1310158402210158401015840W)-F UFMT 18474-5 UFMT18479 MUFMT 18476-8 UFMT 18480-6
Pseudopaludicola saltica Brazil Mato Grosso Chapadados Guimaraes (type-locality 15∘2310158400910158401015840S 55∘5010158402410158401015840W)-MUFMT 482 UFMT 819 UFMT 821 UFMT 823 UFMT 1433-5 UFMT 1437-41 UFMT 2873 UFMT 2877 UFMT 2880-1F UFMT 1442 Cuiaba M UFMT 270 UFMT 473 UFMT476 UFMT 13657-68 F UFMT 13655-6) Nova Lacerda (MUFMT 13499-501) Porto Estrela Estacao Ecologica da Serradas Araras (M UFMT 561) and Vila Bela da SantıssimaTrindade (M UFMT 4082 UFMT 4112 UFMT 4123 UFMT4147 UFMT4153 UFMT4157 UFMT4172)MatoGrosso doSul Sonora (M UFMT 1147 UFMT 1195)
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho (type-locality 20∘0610158403210158401015840S 43∘5810158405310158401015840W)-F MCNAM 3675 MUFMT 18424 UFMT 18451 MCNAM 3677-8 MCNAM3680 Itabirito (20∘1310158402910158401015840S 43∘4810158404910158401015840W)-F MCNAM14620-1 M MCNAM 14625 Lavras Novas (20∘2810158405710158401015840S43∘3010158405210158401015840W)-F MCNAM 3694 M MCNAM 3695MCNAM 3690 Mariana (20∘0910158401210158401015840S 43∘3010158400210158401015840W)-FMCNAM 6465 M MCNAM 6457 MCNAM 6461-2 OuroBranco (20∘3010158401610158401015840S 43∘4210158400410158401015840W)-M MCNAM 6559 SaoJoao Del Rei (21∘0810158402510158401015840S 44∘1710158403110158401015840W)-M UFMT 18425-6UFMT 18452-3 and Botumirim (16∘4410158401310158401015840S 42∘3410158402910158401015840W)-FMCNAM 6713 M MCNAM 6832 MCNAM 6834 MCNAM6636 MCNAM 6642-3
B Analyzed Sound Files
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality) LH 676 no voucher specimen LH 677 call
fromUFMT 18455 LH 678 call fromUFMT 18395 and FNJV12976 no voucher specimen Minas Gerais Sao Roque deMinas (20∘1310158402010158401015840S 46∘2710158402410158401015840W) FNJV 4575 no voucherspecimen and Pocos de Caldas (21∘5510158400410158401015840S 46∘3410158400210158401015840W)FNJV 4576 no voucher specimen
Pseudopaludicola mystacalis Brazil Ceara Itapipoca(03∘2410158405810158401015840S 39∘4110158403110158401015840W) LH 655 no voucher specimenTaiba (03∘2510158404410158401015840S 38∘5710158404310158401015840W) LH 658 no voucher spec-imen Goias Uruacu LH 639 call from UFMT 18410) MatoGrosso Chapada dos Guimaraes (type-locality) LH 13A-05no voucher specimen) Caceres LH 47A-04 call fromUFMT10451 Cuiaba LH 14A-01 call from UFMT 2426 LH 14A-02 call from UFMT 2424 Pocone LH 01A-01 call fromUFMT 4321 and Nossa Senhora do Livramento LH 04A-10 call from UFMT 4330 Maranhao Balsa (07∘2810158404910158401015840S46∘0310158401910158401015840W) LH 284 no voucher specimen Piauı Brejo doPiauı (08∘1110158405010158401015840S 42∘4910158405910158401015840W) LH 184 call from UFMT11202 Para Primavera LH 352 call from UFMT 11836 SaoPaulo Icem LH 701 call from UFMT 18423
Pseudopaludicola saltica BrazilMatoGrossoCuiaba LH13A-01 call fromUFMT 8187Nova Lacerda LH 42A-06 callfrom UFMT 13499 LH 42A-07 call from UFMT 13500 andPorto Estrela LH 12 no voucher specimen LH 13 call fromUFMT 13678 LH 14 call fromUFMT 16423 LH 16 call fromUFMT 16417 LH 17 call from UFMT 16414 and LH 18 callfrom UFMT 16385 Minas Gerais Uberlandia (18∘5810158403010158401015840S48∘1710158402610158401015840W) LH 709 no voucher specimen
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho LH 673call from UFMT 18451 LH 674 no voucher specimen andSao Joao Del Rei LH 675 call from UFMT 18426 and FNJV12879-80 no voucher specimen
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Special thanks go to Felipe Franco Curcio Diva MariaBorges-Nojosa and Luciana Barreto Nascimento for allow-ing access to the material under their care at ldquoColecaoZoologica de Vertebrados da Universidade Federal de MatoGrossordquo (UFMT) ldquoColecao Herpetologica da UniversidadeFederal do Cearardquo (UFC) and ldquoMuseu de Ciencias Naturaisrdquo(MCNAM Belo Horizonte Minas Gerais) respectively toAdao J Cardoso (in memoriam) and Luis F Toledo for therecordings and for allowing access respectively to bioa-coustic samples deposited at ldquoFonoteca Neotropical JacquesVielliardrdquo (FNJV) to the CNPq project ldquoRede de pesquisa emanfıbios e repteis de ecossistemas nao florestais brasileirosrdquo(Process no 5633522010-8) for logistical support to VivianUhlig (RANICMBio) for estimates of extent of occurrenceAndre Pansonato thanks ldquoCoordenacao de Aperfeicoamentode Pessoal de Nivel Superiorrdquo (CAPES) for a PhD scholar-ship and Christine Strussmann thanks CNPq for a researchfellowship (Process no 3095412012-3)
Advances in Zoology 13
References
[1] K D Wells The Ecology amp Behavior of Amphibians TheUniversity of Chicago Chicago Ill USA 2007
[2] M Vences M Gehara J Kohler and F Glaw ldquoDescription of anewMalagasy treefrog (Boophis) occurring syntopically with itssister species and a plea for studies on non-allopatric speciationin tropical amphibiansrdquo Amphibia Reptilia vol 33 no 3-4 pp503ndash520 2012
[3] I De La Riva R Marquez and J Bosch ldquoDescription ofthe advertisement calls of some South American Hylidae(Amphibia Anura) taxonomic and methodological conse-quencesrdquo Bonner Zoologische Beitrage vol 47 pp 175ndash185 1997
[4] F S de Andrade and T R de Carvalho ldquoA new species of Pseu-dopaludicola Miranda-Ribeiro (Leiuperinae LeptodactylidaeAnura) from the Cerrado of southeastern Brazilrdquo Zootaxa vol3608 no 5 pp 389ndash397 2013
[5] D Cardozo and L F Toledo ldquoTaxonomic status of Pseudopalu-dicola riopiedadensis Mercadal de Barrio and Barrio 1994(Anura Leptodactylidae Leiuperinae)rdquo Zootaxa vol 3734 pp571ndash582 2013
[6] T R de Carvalho ldquoA new species of PseudopaludicolaMiranda-Ribeiro (Leiuperinae Leptodactylidae Anura) from the Cer-rado of southeastern Brazil with a distinctive advertisement callpatternrdquo Zootaxa no 3328 pp 47ndash54 2012
[7] F M Magalhaes D Loebmann M N C Kokubum C F BHaddad and A A Garda ldquoA new species of Pseudopaludi-cola (Anura Leptodactylidae Leiuperinae) from NortheasternBrazilrdquo Herpetologica vol 70 pp 77ndash88 2014
[8] A Pansonato C Strussmann J R Mudrek and I A Mar-tins ldquoMorphometric and bioacoustic data on three species ofPseudopaludicola Miranda-Ribeiro 1926 (Anura Leptodactyl-idae Leiuperinae) described from Chapada dos GuimaraesMato Grosso Brazil with the revalidation of Pseudopaludicolaameghini (Cope 1887)rdquo Zootaxa vol 3620 no 1 pp 147ndash1622013
[9] I J Roberto D Cardozo and R W Avila ldquoA new speciesof Pseudopaludicola (Anura Leiuperidae) from Western PiauıState Northeast Brazilrdquo Zootaxa vol 3636 no 2 pp 348ndash3602013
[10] S B Barreto M S Tinoco D Couto-Ferreira and H CBrowne-Ribeiro ldquoDistribuicao de Pseudopaludicola aff falcipes(Anura Leiuperidae) na restinga do litoral norte da BahiaBrasilrdquoRevista Latino-Americana de Conservacao vol 2 pp 27ndash36 2012
[11] E R Favero A C P Veiga-Menoncello D C Rossa-Feres et alldquoIntrageneric karyotypic variation in Pseudopaludicola (AnuraLeiuperidae) and its taxonomic relatednessrdquo Zoological Studiesvol 50 no 6 pp 826ndash836 2011
[12] M Jansen R Bloch A Schulze andM Pfenninger ldquoIntegrativeinventory of Boliviarsquos lowland anurans reveals hidden diversityrdquoZoologica Scripta vol 40 no 6 pp 567ndash583 2011
[13] C P D Prado M Uetanabaro and C F B Haddad ldquoBreed-ing activity patterns reproductive modes and habitat use byanurans (Amphibia) in a seasonal environment in the PantanalBrazilrdquo Amphibia Reptilia vol 26 no 2 pp 211ndash221 2005
[14] R A Silva I A Martins and D C Rossa-Feres ldquoBioacustica esıtio de vocalizacao em taxocenoses de anfıbios de area abertano Noroeste Paulistardquo Biota Neotropica vol 8 pp 123ndash1342008
[15] L F Toledo ldquoDescription of a new species of PseudopaludicolaMiranda-Ribeiro 1926 from the state of Sao Paulo SoutheasternBrazil (Anura Leiuperidae)rdquoZootaxa no 2681 pp 47ndash56 2010
[16] L F Toledo S Siqueira T CDuarte A C P Veiga-MenoncelloS M Recco-Pimentel and C F B Haddad ldquoDescription of anew species of Pseudopaludicola Miranda-Ribeiro 1926 fromthe state of Sao Paulo Southeastern Brazil (Anura Leiuperi-dae)rdquo Zootaxa no 2496 pp 38ndash48 2010
[17] C F B Haddad and A J Cardoso ldquoTaxonomia de tres especiesde Pseudopaludicola (Anura Leptodactylidae)rdquo Papeis Avulsosde Zoologia vol 36 pp 287ndash300 1987
[18] T C Duarte A C P Veiga-Menoncello J F R Lima et alldquoChromosome analysis in Pseudopaludicola (Anura Leiuperi-dae) with description of sex chromosomes XXXY in P salticardquoHereditas vol 147 no 2 pp 43ndash52 2010
[19] A C P Veiga-Menoncello L B Lourenco C Strussmannet al ldquoA phylogenetic analysis of Pseudopaludicola (Anura)providing evidence of progressive chromosome reductionrdquoZoologica Scripta vol 43 no 3 pp 261ndash272 2014
[20] W R Heyer A S Rand C A G Cruz O L Peixoto and CE Nelson ldquoFrogs of Boraceiardquo Arquivos de Zoologia vol 31 pp231ndash410 1990
[21] W E Duellman The Hylid Frogs of Middle America vol 1 ofMonograph of the Museum of Natural History of University ofKansas 1970
[22] R Development Core Team The R Project for Statistical Com-puting Vienna Austria 2013 httpwwwr-projectorg
[23] P E Vanzolini ldquoEcological and geographical distribution oflizards in Pernambuco Northeastern Brasil (Sauria)rdquo PapeisAvulsos de Zoologia vol 18 no 4 pp 61ndash90 1974
[24] J M Cei ldquoAmphibians of Argentinardquo Monitore ZoologicoItaliano Nuova Serie Monografia vol 2 pp 1ndash609 1980
[25] F Brusquetti and E O Lavilla ldquoLista comentada de los anfibiosde ParaguayrdquoCuadernos deHerpetologıa vol 20 no 2 pp 3ndash792006
[26] I De La Riva J Kohler S Lotters and S Reichle ldquoTenyears of research on Bolivian amphibians updated checklistdistribution taxonomic problems literature and iconographyrdquoRevista Espanola Herpetologica vol 14 pp 19ndash164 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
10 Advances in Zoology
4
2
0
minus2
minus4
6420minus2minus4
DF2
(2
)
DF1 (98)
(a)
4
2
0
minus2
minus4
6420minus2minus4
DF2
(1
)
DF1 (99)
(b)
Figure 6 Scatterplots on the two discriminant axes (DF1 and DF2) of scores of 12 morphometric characters of males (a) and six bioacousticvariables (b) of Pseudopaludicola murundu (open circles) P saltica (triangles) and P serrana (closed circles)
Elevation (m)
0
(km)
minus155ndash350351ndash700701ndash1050
1050ndash14001401ndash1750
300
N
1
2
3
4
5
6 78
91011
12
13
Figure 7 Geographical distribution of Pseudopaludicola murundu(circles) and P saltica (triangles) in southeastern Brazil state of SaoPaulomdashRioClaro (type locality (1)) andCampinas (2) state ofMinasGeraismdashPocos de Caldas (3) Alpinopolis (4) (see [17]) Sao Roquede Minas (5) Sao Joao Del Rei (6) Mariana (7) Ouro Branco (8)Itabirito (9) Brumadinho (10) Lavras Novas (11) Botumirim (12)and Uberlandia (13)
variation in the number of notes per minute and in thenumber of pulses in four localities from the state of MatoGrosso is 81 notesmin in Cuiaba and 5 pulsesnote in Cuiabaand Nossa Senhora do Livramento (see Table 3 and [8])Mean note duration does not differ significantly in all theexamined calls (Table 3 119865 = 49 df = 2 119875 = 003)
Table 5 Summary of the number of male specimens correctlyclassified as Pseudopaludicolamurundu P saltica or P serrana usingdiscriminant function analysis of 12 morphometric measurementsand seven bioacoustic variables
Morphometric measurementsTrue group
P murundu P saltica P serranaP murundu 1 0 5P saltica 0 39 0P serrana 3 0 19Total number 6 39 22 16 100 86
Bioacoustic variablesTrue group
P murundu P saltica P serranaP murundu 5 0 1P saltica 0 8 1P serrana 3 0 2Total number 6 9 5 83 889 40
Acoustic analysis of geographical variation in specieswith an extent of occurrence of the magnitude seen inP mystacalis sometimes reveals cryptic taxa being treatedunder a single name However this was not the case in Pmystacalis a taxon that remained erroneously characterizedand poorly recognized in the literature until recently [8] Ourresults reveal a relatively small variation in morphologicaland acoustical traits of P mystacalis and allow confirming thepresence of the species in a wide geographical area along theBrazilian open ecosystems
Advances in Zoology 11
Table 6 Ratios of selected measurements (in mm) of males of Pseudopaludicola murundu P salticaand P serrana Values are presented asmean plusmn standard deviation119873 = number of specimens analyzed
HLSVL HWSVL HLHW HALSVL FLSVL THLSVL TLSVLP serrana (119873 = 21) 040 plusmn 003 036 plusmn 002 110 plusmn 006 027 plusmn 002 061 plusmn 004 056 plusmn 003 070 plusmn 003
P murundu (119873 = 5) 039 plusmn 004 035 plusmn 003 111 plusmn 009 027 plusmn 001 066 plusmn 002 056 plusmn 002 070 plusmn 003
P saltica (119873 = 44) 041 plusmn 004 038 plusmn 003 109 plusmn 011 026 plusmn 003 068 plusmn 006 055 plusmn 005 073 plusmn 005
HAL hand length HL head length HW head width FL foot length SVL snout-vent length THL thigh length TL tibia length
42 Taxonomic Status of Pseudopaludicola serrana Toledo2010 When describing P serrana Toledo [15] used asmorphological characteristics separating the three speciesbelonging to the P saltica group the aspect (relative size andcoloration) of nuptial pads in the external part of finger I andaspect of the vocal sac Such characteristics allow differingP serrana and P murundu from P saltica but do not allowdiffering P serrana from P murundu [15] Previously Haddadand Cardoso [17] had called attention to the fact that nuptialpads were more developed in specimens of P saltica from thetype-locality (Chapada do Guimaraes Mato Grosso) than inspecimens collected and recorded in localities in the statesof Minas Gerais and Sao Paulo In the same article Haddadand Cardoso [17] also presented a spectrogram of the callof a specimen from Campinas Sao Paulo Based on suchreported morphological evidence and acoustic parameterswe here argue that specimens from Minas Gerais and SaoPaulo attributed to P saltica in Haddad and Cardoso [17] infact correspond to P murundu
The only external morphological characteristic used byToledo [15] to differ P serrana from P murunduwas a shorterhead lengthheadwidth ratio (HLHW= 097plusmn006 in the fiveindividuals ofP serrana evaluated 111plusmn007 in 11 individualsof P murundu) After having analyzed a higher number ofspecimens attributed to P serrana (119873 = 21) we found thatHLHW (110 plusmn 006 see Table 6) in this sample does notdiffer from the values presented in the original descriptionand confirmed herein for P murundu
The description of P serrana was also based on physicalcharacteristics of its advertisement calls [15] However theoriginal dataset is relatively low 12 notes of a single maleof P saltica 14 notes of 2 males of P murundu and 15notes of 3 males of P serrana were analyzed and comparedOnly one out of four acoustic variables (pulse duration) wasconsidered diagnostic for the new species Toledo [15] alsoshowed that dominant frequency range of P serrana wascompletely nested within the dominant frequency range of Pmurundu However when later proposing the synonymiza-tion of Pseudopaludicola riopiedadensis Mercadal de Bar-rio and Barrio 1994 to Pseudopaludicola ternetzi Miranda-Ribeiro 1937 Cardozo and Toledo [5] based their decision onldquoseveral important overlapsrdquo including dominant frequencyranges between the two species Indeed our data showedthat dominant frequency contributed to higher loadingsto separate species in the P saltica group Nonoverlappingdominant frequencies would therefore be expected betweenrelated but distinct species of Pseudopaludicola
Bioacoustic data have proven to be useful for uncoveringmorphologically cryptic species in the genus Pseudopaludi-cola [4ndash9 15 16] Advertisement calls of species in this genusmight be divided into three distinct groups according to typeof notes nonpulsed notes notes with concatenated pulsesand noteswith nonconcatenated pulses [7] Each groupmightbe diagnosed by temporal (pulses per note note and pulseduration internotes and interpulses intervals note rate andpulse rate) and spectral variables (dominant frequency andharmonics) which in combination allow characterizing allthe species for which calls were already analyzed except forP serrana and P murundu As evidenced by the recent syn-onymization of Pseudopaludicola riopiedadensis to P ternetzi[15] and reinforced herein by the proposed synonymizationof P serrana to P murundu morphologically similar speciesof Pseudopaludicola presenting the same type of note and anoverlap in their spectral acoustic variables are expected torepresent the same taxon Therefore no arguments remainto consider P serrana as a distinct species from P murunduand the former must be considered as a junior synonym of Pmurundu
5 Conclusions
We here report on the variation in morphometric charactersand variation in bioacoustic variables of the advertisementcalls in fifteen Brazilian populations of Pseudopaludicolamys-tacalis Although limited our sample evidenced no statisticaldifferences in any of the evaluated attributes and allowed usto confirm that this species is widely distributed in BrazilMorphometric and bioacoustic data did not differ also inpopulations currently attributed to Pseudopaludicola serranaand Pseudopaludicola murundu and the former taxon ishere considered as a junior synonym of P murundu Thedata in the present work aims at contributing to a betterunderstanding of the diversity and distribution patterns inthe genus Pseudopaludicola
Appendices
A Voucher Specimens Examined
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality 22∘1910158405210158401015840S 47∘4210158405610158401015840W)-F UFMT 18454MUFMT 18395-6 UFMT 18455-7
Pseudopaludicola mystacalis Brazil Para Primavera(00∘5710158402210158401015840S 47∘0710158401210158401015840W)-M UFMT 11651 UFMT 11827
12 Advances in Zoology
UFMT 11833 UFMT 11836 UFMT 11839 Goias Uruacu(14∘3110158403510158401015840S 49∘0710158405410158401015840W)-F UFMT 18397-400 UFMT18458-9 M UFMT 18401-15 UFMT 18458-64 Mato GrossoBarra do Garcas (15∘3110158405710158401015840S 52∘1410158401010158401015840W)-M UFMT11097 UFMT 11307 UFMT 11319 UFMT 11324 Caceres(16∘1710158405910158401015840S 58∘0910158400910158401015840W)-F UFMT 5906 UFMT 5950UFMT 5955 UFMT 5962 UFMT 9152 UFMT 10445UFMT 10448 UFMT 13669 M UFMT 10451-2 UFMT10455 UFMT 10458 UFMT 10466 UFMT 10495 UFMT10506 UFMT 10508 UFMT 13670 Chapada dos Guimaraes(type-locality 14∘5010158403410158401015840S 55∘2310158401010158401015840W)-F UFMT 8109 MUFMT 487 UFMT 817 UFMT 820 UFMT 12890 Cuiaba(15∘3910158403310158401015840S 55∘5610158403010158401015840W)-M UFMT 15980 UFMT 2426UFMT 2430 UFMT 2432 UFMT 2434-7 UFMT 2439UFMT 7399 UFMT 7653 UFMT 8177-8 UFMT 8180UFMT 8182 UFMT 8184-5 UFMT 13671 Nossa Senhorado Livramento (16∘2110158405810158401015840S 56∘1810158403310158401015840W)-F UFMT 18465UFMT 352 UFMT 6436 UFMT 6466-7 UFMT 6488UFMT 6511 M UFMT 4343 UFMT 6487 UFMT 6491UFMT6498UFMT6515Pocone (16∘3010158405810158401015840S 56∘4410158405310158401015840W)-M UFMT 348-50 UFMT 889 UFMT 4316 UFMT 4318UFMT 4321 UFMT 13672 and Porto Estrela (15∘3510158400510158401015840S57∘1310158402010158401015840W)-F UFMT 18466-7 UFMT 138 UFMT 13482M UFMT 18468-9 UFMT 402 UFMT 2200 UFMT 11346Sao Paulo Icem (20∘2010158403110158401015840S 49∘1110158404210158401015840W)-F UFMT 18421UFMT 18470-2 M UFMT 18422-3 UFMT 18473 and AltoAlegre (21∘3310158402010158401015840S 50∘1310158402210158401015840W)-F UFMT 18474-5 UFMT18479 MUFMT 18476-8 UFMT 18480-6
Pseudopaludicola saltica Brazil Mato Grosso Chapadados Guimaraes (type-locality 15∘2310158400910158401015840S 55∘5010158402410158401015840W)-MUFMT 482 UFMT 819 UFMT 821 UFMT 823 UFMT 1433-5 UFMT 1437-41 UFMT 2873 UFMT 2877 UFMT 2880-1F UFMT 1442 Cuiaba M UFMT 270 UFMT 473 UFMT476 UFMT 13657-68 F UFMT 13655-6) Nova Lacerda (MUFMT 13499-501) Porto Estrela Estacao Ecologica da Serradas Araras (M UFMT 561) and Vila Bela da SantıssimaTrindade (M UFMT 4082 UFMT 4112 UFMT 4123 UFMT4147 UFMT4153 UFMT4157 UFMT4172)MatoGrosso doSul Sonora (M UFMT 1147 UFMT 1195)
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho (type-locality 20∘0610158403210158401015840S 43∘5810158405310158401015840W)-F MCNAM 3675 MUFMT 18424 UFMT 18451 MCNAM 3677-8 MCNAM3680 Itabirito (20∘1310158402910158401015840S 43∘4810158404910158401015840W)-F MCNAM14620-1 M MCNAM 14625 Lavras Novas (20∘2810158405710158401015840S43∘3010158405210158401015840W)-F MCNAM 3694 M MCNAM 3695MCNAM 3690 Mariana (20∘0910158401210158401015840S 43∘3010158400210158401015840W)-FMCNAM 6465 M MCNAM 6457 MCNAM 6461-2 OuroBranco (20∘3010158401610158401015840S 43∘4210158400410158401015840W)-M MCNAM 6559 SaoJoao Del Rei (21∘0810158402510158401015840S 44∘1710158403110158401015840W)-M UFMT 18425-6UFMT 18452-3 and Botumirim (16∘4410158401310158401015840S 42∘3410158402910158401015840W)-FMCNAM 6713 M MCNAM 6832 MCNAM 6834 MCNAM6636 MCNAM 6642-3
B Analyzed Sound Files
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality) LH 676 no voucher specimen LH 677 call
fromUFMT 18455 LH 678 call fromUFMT 18395 and FNJV12976 no voucher specimen Minas Gerais Sao Roque deMinas (20∘1310158402010158401015840S 46∘2710158402410158401015840W) FNJV 4575 no voucherspecimen and Pocos de Caldas (21∘5510158400410158401015840S 46∘3410158400210158401015840W)FNJV 4576 no voucher specimen
Pseudopaludicola mystacalis Brazil Ceara Itapipoca(03∘2410158405810158401015840S 39∘4110158403110158401015840W) LH 655 no voucher specimenTaiba (03∘2510158404410158401015840S 38∘5710158404310158401015840W) LH 658 no voucher spec-imen Goias Uruacu LH 639 call from UFMT 18410) MatoGrosso Chapada dos Guimaraes (type-locality) LH 13A-05no voucher specimen) Caceres LH 47A-04 call fromUFMT10451 Cuiaba LH 14A-01 call from UFMT 2426 LH 14A-02 call from UFMT 2424 Pocone LH 01A-01 call fromUFMT 4321 and Nossa Senhora do Livramento LH 04A-10 call from UFMT 4330 Maranhao Balsa (07∘2810158404910158401015840S46∘0310158401910158401015840W) LH 284 no voucher specimen Piauı Brejo doPiauı (08∘1110158405010158401015840S 42∘4910158405910158401015840W) LH 184 call from UFMT11202 Para Primavera LH 352 call from UFMT 11836 SaoPaulo Icem LH 701 call from UFMT 18423
Pseudopaludicola saltica BrazilMatoGrossoCuiaba LH13A-01 call fromUFMT 8187Nova Lacerda LH 42A-06 callfrom UFMT 13499 LH 42A-07 call from UFMT 13500 andPorto Estrela LH 12 no voucher specimen LH 13 call fromUFMT 13678 LH 14 call fromUFMT 16423 LH 16 call fromUFMT 16417 LH 17 call from UFMT 16414 and LH 18 callfrom UFMT 16385 Minas Gerais Uberlandia (18∘5810158403010158401015840S48∘1710158402610158401015840W) LH 709 no voucher specimen
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho LH 673call from UFMT 18451 LH 674 no voucher specimen andSao Joao Del Rei LH 675 call from UFMT 18426 and FNJV12879-80 no voucher specimen
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Special thanks go to Felipe Franco Curcio Diva MariaBorges-Nojosa and Luciana Barreto Nascimento for allow-ing access to the material under their care at ldquoColecaoZoologica de Vertebrados da Universidade Federal de MatoGrossordquo (UFMT) ldquoColecao Herpetologica da UniversidadeFederal do Cearardquo (UFC) and ldquoMuseu de Ciencias Naturaisrdquo(MCNAM Belo Horizonte Minas Gerais) respectively toAdao J Cardoso (in memoriam) and Luis F Toledo for therecordings and for allowing access respectively to bioa-coustic samples deposited at ldquoFonoteca Neotropical JacquesVielliardrdquo (FNJV) to the CNPq project ldquoRede de pesquisa emanfıbios e repteis de ecossistemas nao florestais brasileirosrdquo(Process no 5633522010-8) for logistical support to VivianUhlig (RANICMBio) for estimates of extent of occurrenceAndre Pansonato thanks ldquoCoordenacao de Aperfeicoamentode Pessoal de Nivel Superiorrdquo (CAPES) for a PhD scholar-ship and Christine Strussmann thanks CNPq for a researchfellowship (Process no 3095412012-3)
Advances in Zoology 13
References
[1] K D Wells The Ecology amp Behavior of Amphibians TheUniversity of Chicago Chicago Ill USA 2007
[2] M Vences M Gehara J Kohler and F Glaw ldquoDescription of anewMalagasy treefrog (Boophis) occurring syntopically with itssister species and a plea for studies on non-allopatric speciationin tropical amphibiansrdquo Amphibia Reptilia vol 33 no 3-4 pp503ndash520 2012
[3] I De La Riva R Marquez and J Bosch ldquoDescription ofthe advertisement calls of some South American Hylidae(Amphibia Anura) taxonomic and methodological conse-quencesrdquo Bonner Zoologische Beitrage vol 47 pp 175ndash185 1997
[4] F S de Andrade and T R de Carvalho ldquoA new species of Pseu-dopaludicola Miranda-Ribeiro (Leiuperinae LeptodactylidaeAnura) from the Cerrado of southeastern Brazilrdquo Zootaxa vol3608 no 5 pp 389ndash397 2013
[5] D Cardozo and L F Toledo ldquoTaxonomic status of Pseudopalu-dicola riopiedadensis Mercadal de Barrio and Barrio 1994(Anura Leptodactylidae Leiuperinae)rdquo Zootaxa vol 3734 pp571ndash582 2013
[6] T R de Carvalho ldquoA new species of PseudopaludicolaMiranda-Ribeiro (Leiuperinae Leptodactylidae Anura) from the Cer-rado of southeastern Brazil with a distinctive advertisement callpatternrdquo Zootaxa no 3328 pp 47ndash54 2012
[7] F M Magalhaes D Loebmann M N C Kokubum C F BHaddad and A A Garda ldquoA new species of Pseudopaludi-cola (Anura Leptodactylidae Leiuperinae) from NortheasternBrazilrdquo Herpetologica vol 70 pp 77ndash88 2014
[8] A Pansonato C Strussmann J R Mudrek and I A Mar-tins ldquoMorphometric and bioacoustic data on three species ofPseudopaludicola Miranda-Ribeiro 1926 (Anura Leptodactyl-idae Leiuperinae) described from Chapada dos GuimaraesMato Grosso Brazil with the revalidation of Pseudopaludicolaameghini (Cope 1887)rdquo Zootaxa vol 3620 no 1 pp 147ndash1622013
[9] I J Roberto D Cardozo and R W Avila ldquoA new speciesof Pseudopaludicola (Anura Leiuperidae) from Western PiauıState Northeast Brazilrdquo Zootaxa vol 3636 no 2 pp 348ndash3602013
[10] S B Barreto M S Tinoco D Couto-Ferreira and H CBrowne-Ribeiro ldquoDistribuicao de Pseudopaludicola aff falcipes(Anura Leiuperidae) na restinga do litoral norte da BahiaBrasilrdquoRevista Latino-Americana de Conservacao vol 2 pp 27ndash36 2012
[11] E R Favero A C P Veiga-Menoncello D C Rossa-Feres et alldquoIntrageneric karyotypic variation in Pseudopaludicola (AnuraLeiuperidae) and its taxonomic relatednessrdquo Zoological Studiesvol 50 no 6 pp 826ndash836 2011
[12] M Jansen R Bloch A Schulze andM Pfenninger ldquoIntegrativeinventory of Boliviarsquos lowland anurans reveals hidden diversityrdquoZoologica Scripta vol 40 no 6 pp 567ndash583 2011
[13] C P D Prado M Uetanabaro and C F B Haddad ldquoBreed-ing activity patterns reproductive modes and habitat use byanurans (Amphibia) in a seasonal environment in the PantanalBrazilrdquo Amphibia Reptilia vol 26 no 2 pp 211ndash221 2005
[14] R A Silva I A Martins and D C Rossa-Feres ldquoBioacustica esıtio de vocalizacao em taxocenoses de anfıbios de area abertano Noroeste Paulistardquo Biota Neotropica vol 8 pp 123ndash1342008
[15] L F Toledo ldquoDescription of a new species of PseudopaludicolaMiranda-Ribeiro 1926 from the state of Sao Paulo SoutheasternBrazil (Anura Leiuperidae)rdquoZootaxa no 2681 pp 47ndash56 2010
[16] L F Toledo S Siqueira T CDuarte A C P Veiga-MenoncelloS M Recco-Pimentel and C F B Haddad ldquoDescription of anew species of Pseudopaludicola Miranda-Ribeiro 1926 fromthe state of Sao Paulo Southeastern Brazil (Anura Leiuperi-dae)rdquo Zootaxa no 2496 pp 38ndash48 2010
[17] C F B Haddad and A J Cardoso ldquoTaxonomia de tres especiesde Pseudopaludicola (Anura Leptodactylidae)rdquo Papeis Avulsosde Zoologia vol 36 pp 287ndash300 1987
[18] T C Duarte A C P Veiga-Menoncello J F R Lima et alldquoChromosome analysis in Pseudopaludicola (Anura Leiuperi-dae) with description of sex chromosomes XXXY in P salticardquoHereditas vol 147 no 2 pp 43ndash52 2010
[19] A C P Veiga-Menoncello L B Lourenco C Strussmannet al ldquoA phylogenetic analysis of Pseudopaludicola (Anura)providing evidence of progressive chromosome reductionrdquoZoologica Scripta vol 43 no 3 pp 261ndash272 2014
[20] W R Heyer A S Rand C A G Cruz O L Peixoto and CE Nelson ldquoFrogs of Boraceiardquo Arquivos de Zoologia vol 31 pp231ndash410 1990
[21] W E Duellman The Hylid Frogs of Middle America vol 1 ofMonograph of the Museum of Natural History of University ofKansas 1970
[22] R Development Core Team The R Project for Statistical Com-puting Vienna Austria 2013 httpwwwr-projectorg
[23] P E Vanzolini ldquoEcological and geographical distribution oflizards in Pernambuco Northeastern Brasil (Sauria)rdquo PapeisAvulsos de Zoologia vol 18 no 4 pp 61ndash90 1974
[24] J M Cei ldquoAmphibians of Argentinardquo Monitore ZoologicoItaliano Nuova Serie Monografia vol 2 pp 1ndash609 1980
[25] F Brusquetti and E O Lavilla ldquoLista comentada de los anfibiosde ParaguayrdquoCuadernos deHerpetologıa vol 20 no 2 pp 3ndash792006
[26] I De La Riva J Kohler S Lotters and S Reichle ldquoTenyears of research on Bolivian amphibians updated checklistdistribution taxonomic problems literature and iconographyrdquoRevista Espanola Herpetologica vol 14 pp 19ndash164 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
Advances in Zoology 11
Table 6 Ratios of selected measurements (in mm) of males of Pseudopaludicola murundu P salticaand P serrana Values are presented asmean plusmn standard deviation119873 = number of specimens analyzed
HLSVL HWSVL HLHW HALSVL FLSVL THLSVL TLSVLP serrana (119873 = 21) 040 plusmn 003 036 plusmn 002 110 plusmn 006 027 plusmn 002 061 plusmn 004 056 plusmn 003 070 plusmn 003
P murundu (119873 = 5) 039 plusmn 004 035 plusmn 003 111 plusmn 009 027 plusmn 001 066 plusmn 002 056 plusmn 002 070 plusmn 003
P saltica (119873 = 44) 041 plusmn 004 038 plusmn 003 109 plusmn 011 026 plusmn 003 068 plusmn 006 055 plusmn 005 073 plusmn 005
HAL hand length HL head length HW head width FL foot length SVL snout-vent length THL thigh length TL tibia length
42 Taxonomic Status of Pseudopaludicola serrana Toledo2010 When describing P serrana Toledo [15] used asmorphological characteristics separating the three speciesbelonging to the P saltica group the aspect (relative size andcoloration) of nuptial pads in the external part of finger I andaspect of the vocal sac Such characteristics allow differingP serrana and P murundu from P saltica but do not allowdiffering P serrana from P murundu [15] Previously Haddadand Cardoso [17] had called attention to the fact that nuptialpads were more developed in specimens of P saltica from thetype-locality (Chapada do Guimaraes Mato Grosso) than inspecimens collected and recorded in localities in the statesof Minas Gerais and Sao Paulo In the same article Haddadand Cardoso [17] also presented a spectrogram of the callof a specimen from Campinas Sao Paulo Based on suchreported morphological evidence and acoustic parameterswe here argue that specimens from Minas Gerais and SaoPaulo attributed to P saltica in Haddad and Cardoso [17] infact correspond to P murundu
The only external morphological characteristic used byToledo [15] to differ P serrana from P murunduwas a shorterhead lengthheadwidth ratio (HLHW= 097plusmn006 in the fiveindividuals ofP serrana evaluated 111plusmn007 in 11 individualsof P murundu) After having analyzed a higher number ofspecimens attributed to P serrana (119873 = 21) we found thatHLHW (110 plusmn 006 see Table 6) in this sample does notdiffer from the values presented in the original descriptionand confirmed herein for P murundu
The description of P serrana was also based on physicalcharacteristics of its advertisement calls [15] However theoriginal dataset is relatively low 12 notes of a single maleof P saltica 14 notes of 2 males of P murundu and 15notes of 3 males of P serrana were analyzed and comparedOnly one out of four acoustic variables (pulse duration) wasconsidered diagnostic for the new species Toledo [15] alsoshowed that dominant frequency range of P serrana wascompletely nested within the dominant frequency range of Pmurundu However when later proposing the synonymiza-tion of Pseudopaludicola riopiedadensis Mercadal de Bar-rio and Barrio 1994 to Pseudopaludicola ternetzi Miranda-Ribeiro 1937 Cardozo and Toledo [5] based their decision onldquoseveral important overlapsrdquo including dominant frequencyranges between the two species Indeed our data showedthat dominant frequency contributed to higher loadingsto separate species in the P saltica group Nonoverlappingdominant frequencies would therefore be expected betweenrelated but distinct species of Pseudopaludicola
Bioacoustic data have proven to be useful for uncoveringmorphologically cryptic species in the genus Pseudopaludi-cola [4ndash9 15 16] Advertisement calls of species in this genusmight be divided into three distinct groups according to typeof notes nonpulsed notes notes with concatenated pulsesand noteswith nonconcatenated pulses [7] Each groupmightbe diagnosed by temporal (pulses per note note and pulseduration internotes and interpulses intervals note rate andpulse rate) and spectral variables (dominant frequency andharmonics) which in combination allow characterizing allthe species for which calls were already analyzed except forP serrana and P murundu As evidenced by the recent syn-onymization of Pseudopaludicola riopiedadensis to P ternetzi[15] and reinforced herein by the proposed synonymizationof P serrana to P murundu morphologically similar speciesof Pseudopaludicola presenting the same type of note and anoverlap in their spectral acoustic variables are expected torepresent the same taxon Therefore no arguments remainto consider P serrana as a distinct species from P murunduand the former must be considered as a junior synonym of Pmurundu
5 Conclusions
We here report on the variation in morphometric charactersand variation in bioacoustic variables of the advertisementcalls in fifteen Brazilian populations of Pseudopaludicolamys-tacalis Although limited our sample evidenced no statisticaldifferences in any of the evaluated attributes and allowed usto confirm that this species is widely distributed in BrazilMorphometric and bioacoustic data did not differ also inpopulations currently attributed to Pseudopaludicola serranaand Pseudopaludicola murundu and the former taxon ishere considered as a junior synonym of P murundu Thedata in the present work aims at contributing to a betterunderstanding of the diversity and distribution patterns inthe genus Pseudopaludicola
Appendices
A Voucher Specimens Examined
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality 22∘1910158405210158401015840S 47∘4210158405610158401015840W)-F UFMT 18454MUFMT 18395-6 UFMT 18455-7
Pseudopaludicola mystacalis Brazil Para Primavera(00∘5710158402210158401015840S 47∘0710158401210158401015840W)-M UFMT 11651 UFMT 11827
12 Advances in Zoology
UFMT 11833 UFMT 11836 UFMT 11839 Goias Uruacu(14∘3110158403510158401015840S 49∘0710158405410158401015840W)-F UFMT 18397-400 UFMT18458-9 M UFMT 18401-15 UFMT 18458-64 Mato GrossoBarra do Garcas (15∘3110158405710158401015840S 52∘1410158401010158401015840W)-M UFMT11097 UFMT 11307 UFMT 11319 UFMT 11324 Caceres(16∘1710158405910158401015840S 58∘0910158400910158401015840W)-F UFMT 5906 UFMT 5950UFMT 5955 UFMT 5962 UFMT 9152 UFMT 10445UFMT 10448 UFMT 13669 M UFMT 10451-2 UFMT10455 UFMT 10458 UFMT 10466 UFMT 10495 UFMT10506 UFMT 10508 UFMT 13670 Chapada dos Guimaraes(type-locality 14∘5010158403410158401015840S 55∘2310158401010158401015840W)-F UFMT 8109 MUFMT 487 UFMT 817 UFMT 820 UFMT 12890 Cuiaba(15∘3910158403310158401015840S 55∘5610158403010158401015840W)-M UFMT 15980 UFMT 2426UFMT 2430 UFMT 2432 UFMT 2434-7 UFMT 2439UFMT 7399 UFMT 7653 UFMT 8177-8 UFMT 8180UFMT 8182 UFMT 8184-5 UFMT 13671 Nossa Senhorado Livramento (16∘2110158405810158401015840S 56∘1810158403310158401015840W)-F UFMT 18465UFMT 352 UFMT 6436 UFMT 6466-7 UFMT 6488UFMT 6511 M UFMT 4343 UFMT 6487 UFMT 6491UFMT6498UFMT6515Pocone (16∘3010158405810158401015840S 56∘4410158405310158401015840W)-M UFMT 348-50 UFMT 889 UFMT 4316 UFMT 4318UFMT 4321 UFMT 13672 and Porto Estrela (15∘3510158400510158401015840S57∘1310158402010158401015840W)-F UFMT 18466-7 UFMT 138 UFMT 13482M UFMT 18468-9 UFMT 402 UFMT 2200 UFMT 11346Sao Paulo Icem (20∘2010158403110158401015840S 49∘1110158404210158401015840W)-F UFMT 18421UFMT 18470-2 M UFMT 18422-3 UFMT 18473 and AltoAlegre (21∘3310158402010158401015840S 50∘1310158402210158401015840W)-F UFMT 18474-5 UFMT18479 MUFMT 18476-8 UFMT 18480-6
Pseudopaludicola saltica Brazil Mato Grosso Chapadados Guimaraes (type-locality 15∘2310158400910158401015840S 55∘5010158402410158401015840W)-MUFMT 482 UFMT 819 UFMT 821 UFMT 823 UFMT 1433-5 UFMT 1437-41 UFMT 2873 UFMT 2877 UFMT 2880-1F UFMT 1442 Cuiaba M UFMT 270 UFMT 473 UFMT476 UFMT 13657-68 F UFMT 13655-6) Nova Lacerda (MUFMT 13499-501) Porto Estrela Estacao Ecologica da Serradas Araras (M UFMT 561) and Vila Bela da SantıssimaTrindade (M UFMT 4082 UFMT 4112 UFMT 4123 UFMT4147 UFMT4153 UFMT4157 UFMT4172)MatoGrosso doSul Sonora (M UFMT 1147 UFMT 1195)
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho (type-locality 20∘0610158403210158401015840S 43∘5810158405310158401015840W)-F MCNAM 3675 MUFMT 18424 UFMT 18451 MCNAM 3677-8 MCNAM3680 Itabirito (20∘1310158402910158401015840S 43∘4810158404910158401015840W)-F MCNAM14620-1 M MCNAM 14625 Lavras Novas (20∘2810158405710158401015840S43∘3010158405210158401015840W)-F MCNAM 3694 M MCNAM 3695MCNAM 3690 Mariana (20∘0910158401210158401015840S 43∘3010158400210158401015840W)-FMCNAM 6465 M MCNAM 6457 MCNAM 6461-2 OuroBranco (20∘3010158401610158401015840S 43∘4210158400410158401015840W)-M MCNAM 6559 SaoJoao Del Rei (21∘0810158402510158401015840S 44∘1710158403110158401015840W)-M UFMT 18425-6UFMT 18452-3 and Botumirim (16∘4410158401310158401015840S 42∘3410158402910158401015840W)-FMCNAM 6713 M MCNAM 6832 MCNAM 6834 MCNAM6636 MCNAM 6642-3
B Analyzed Sound Files
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality) LH 676 no voucher specimen LH 677 call
fromUFMT 18455 LH 678 call fromUFMT 18395 and FNJV12976 no voucher specimen Minas Gerais Sao Roque deMinas (20∘1310158402010158401015840S 46∘2710158402410158401015840W) FNJV 4575 no voucherspecimen and Pocos de Caldas (21∘5510158400410158401015840S 46∘3410158400210158401015840W)FNJV 4576 no voucher specimen
Pseudopaludicola mystacalis Brazil Ceara Itapipoca(03∘2410158405810158401015840S 39∘4110158403110158401015840W) LH 655 no voucher specimenTaiba (03∘2510158404410158401015840S 38∘5710158404310158401015840W) LH 658 no voucher spec-imen Goias Uruacu LH 639 call from UFMT 18410) MatoGrosso Chapada dos Guimaraes (type-locality) LH 13A-05no voucher specimen) Caceres LH 47A-04 call fromUFMT10451 Cuiaba LH 14A-01 call from UFMT 2426 LH 14A-02 call from UFMT 2424 Pocone LH 01A-01 call fromUFMT 4321 and Nossa Senhora do Livramento LH 04A-10 call from UFMT 4330 Maranhao Balsa (07∘2810158404910158401015840S46∘0310158401910158401015840W) LH 284 no voucher specimen Piauı Brejo doPiauı (08∘1110158405010158401015840S 42∘4910158405910158401015840W) LH 184 call from UFMT11202 Para Primavera LH 352 call from UFMT 11836 SaoPaulo Icem LH 701 call from UFMT 18423
Pseudopaludicola saltica BrazilMatoGrossoCuiaba LH13A-01 call fromUFMT 8187Nova Lacerda LH 42A-06 callfrom UFMT 13499 LH 42A-07 call from UFMT 13500 andPorto Estrela LH 12 no voucher specimen LH 13 call fromUFMT 13678 LH 14 call fromUFMT 16423 LH 16 call fromUFMT 16417 LH 17 call from UFMT 16414 and LH 18 callfrom UFMT 16385 Minas Gerais Uberlandia (18∘5810158403010158401015840S48∘1710158402610158401015840W) LH 709 no voucher specimen
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho LH 673call from UFMT 18451 LH 674 no voucher specimen andSao Joao Del Rei LH 675 call from UFMT 18426 and FNJV12879-80 no voucher specimen
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Special thanks go to Felipe Franco Curcio Diva MariaBorges-Nojosa and Luciana Barreto Nascimento for allow-ing access to the material under their care at ldquoColecaoZoologica de Vertebrados da Universidade Federal de MatoGrossordquo (UFMT) ldquoColecao Herpetologica da UniversidadeFederal do Cearardquo (UFC) and ldquoMuseu de Ciencias Naturaisrdquo(MCNAM Belo Horizonte Minas Gerais) respectively toAdao J Cardoso (in memoriam) and Luis F Toledo for therecordings and for allowing access respectively to bioa-coustic samples deposited at ldquoFonoteca Neotropical JacquesVielliardrdquo (FNJV) to the CNPq project ldquoRede de pesquisa emanfıbios e repteis de ecossistemas nao florestais brasileirosrdquo(Process no 5633522010-8) for logistical support to VivianUhlig (RANICMBio) for estimates of extent of occurrenceAndre Pansonato thanks ldquoCoordenacao de Aperfeicoamentode Pessoal de Nivel Superiorrdquo (CAPES) for a PhD scholar-ship and Christine Strussmann thanks CNPq for a researchfellowship (Process no 3095412012-3)
Advances in Zoology 13
References
[1] K D Wells The Ecology amp Behavior of Amphibians TheUniversity of Chicago Chicago Ill USA 2007
[2] M Vences M Gehara J Kohler and F Glaw ldquoDescription of anewMalagasy treefrog (Boophis) occurring syntopically with itssister species and a plea for studies on non-allopatric speciationin tropical amphibiansrdquo Amphibia Reptilia vol 33 no 3-4 pp503ndash520 2012
[3] I De La Riva R Marquez and J Bosch ldquoDescription ofthe advertisement calls of some South American Hylidae(Amphibia Anura) taxonomic and methodological conse-quencesrdquo Bonner Zoologische Beitrage vol 47 pp 175ndash185 1997
[4] F S de Andrade and T R de Carvalho ldquoA new species of Pseu-dopaludicola Miranda-Ribeiro (Leiuperinae LeptodactylidaeAnura) from the Cerrado of southeastern Brazilrdquo Zootaxa vol3608 no 5 pp 389ndash397 2013
[5] D Cardozo and L F Toledo ldquoTaxonomic status of Pseudopalu-dicola riopiedadensis Mercadal de Barrio and Barrio 1994(Anura Leptodactylidae Leiuperinae)rdquo Zootaxa vol 3734 pp571ndash582 2013
[6] T R de Carvalho ldquoA new species of PseudopaludicolaMiranda-Ribeiro (Leiuperinae Leptodactylidae Anura) from the Cer-rado of southeastern Brazil with a distinctive advertisement callpatternrdquo Zootaxa no 3328 pp 47ndash54 2012
[7] F M Magalhaes D Loebmann M N C Kokubum C F BHaddad and A A Garda ldquoA new species of Pseudopaludi-cola (Anura Leptodactylidae Leiuperinae) from NortheasternBrazilrdquo Herpetologica vol 70 pp 77ndash88 2014
[8] A Pansonato C Strussmann J R Mudrek and I A Mar-tins ldquoMorphometric and bioacoustic data on three species ofPseudopaludicola Miranda-Ribeiro 1926 (Anura Leptodactyl-idae Leiuperinae) described from Chapada dos GuimaraesMato Grosso Brazil with the revalidation of Pseudopaludicolaameghini (Cope 1887)rdquo Zootaxa vol 3620 no 1 pp 147ndash1622013
[9] I J Roberto D Cardozo and R W Avila ldquoA new speciesof Pseudopaludicola (Anura Leiuperidae) from Western PiauıState Northeast Brazilrdquo Zootaxa vol 3636 no 2 pp 348ndash3602013
[10] S B Barreto M S Tinoco D Couto-Ferreira and H CBrowne-Ribeiro ldquoDistribuicao de Pseudopaludicola aff falcipes(Anura Leiuperidae) na restinga do litoral norte da BahiaBrasilrdquoRevista Latino-Americana de Conservacao vol 2 pp 27ndash36 2012
[11] E R Favero A C P Veiga-Menoncello D C Rossa-Feres et alldquoIntrageneric karyotypic variation in Pseudopaludicola (AnuraLeiuperidae) and its taxonomic relatednessrdquo Zoological Studiesvol 50 no 6 pp 826ndash836 2011
[12] M Jansen R Bloch A Schulze andM Pfenninger ldquoIntegrativeinventory of Boliviarsquos lowland anurans reveals hidden diversityrdquoZoologica Scripta vol 40 no 6 pp 567ndash583 2011
[13] C P D Prado M Uetanabaro and C F B Haddad ldquoBreed-ing activity patterns reproductive modes and habitat use byanurans (Amphibia) in a seasonal environment in the PantanalBrazilrdquo Amphibia Reptilia vol 26 no 2 pp 211ndash221 2005
[14] R A Silva I A Martins and D C Rossa-Feres ldquoBioacustica esıtio de vocalizacao em taxocenoses de anfıbios de area abertano Noroeste Paulistardquo Biota Neotropica vol 8 pp 123ndash1342008
[15] L F Toledo ldquoDescription of a new species of PseudopaludicolaMiranda-Ribeiro 1926 from the state of Sao Paulo SoutheasternBrazil (Anura Leiuperidae)rdquoZootaxa no 2681 pp 47ndash56 2010
[16] L F Toledo S Siqueira T CDuarte A C P Veiga-MenoncelloS M Recco-Pimentel and C F B Haddad ldquoDescription of anew species of Pseudopaludicola Miranda-Ribeiro 1926 fromthe state of Sao Paulo Southeastern Brazil (Anura Leiuperi-dae)rdquo Zootaxa no 2496 pp 38ndash48 2010
[17] C F B Haddad and A J Cardoso ldquoTaxonomia de tres especiesde Pseudopaludicola (Anura Leptodactylidae)rdquo Papeis Avulsosde Zoologia vol 36 pp 287ndash300 1987
[18] T C Duarte A C P Veiga-Menoncello J F R Lima et alldquoChromosome analysis in Pseudopaludicola (Anura Leiuperi-dae) with description of sex chromosomes XXXY in P salticardquoHereditas vol 147 no 2 pp 43ndash52 2010
[19] A C P Veiga-Menoncello L B Lourenco C Strussmannet al ldquoA phylogenetic analysis of Pseudopaludicola (Anura)providing evidence of progressive chromosome reductionrdquoZoologica Scripta vol 43 no 3 pp 261ndash272 2014
[20] W R Heyer A S Rand C A G Cruz O L Peixoto and CE Nelson ldquoFrogs of Boraceiardquo Arquivos de Zoologia vol 31 pp231ndash410 1990
[21] W E Duellman The Hylid Frogs of Middle America vol 1 ofMonograph of the Museum of Natural History of University ofKansas 1970
[22] R Development Core Team The R Project for Statistical Com-puting Vienna Austria 2013 httpwwwr-projectorg
[23] P E Vanzolini ldquoEcological and geographical distribution oflizards in Pernambuco Northeastern Brasil (Sauria)rdquo PapeisAvulsos de Zoologia vol 18 no 4 pp 61ndash90 1974
[24] J M Cei ldquoAmphibians of Argentinardquo Monitore ZoologicoItaliano Nuova Serie Monografia vol 2 pp 1ndash609 1980
[25] F Brusquetti and E O Lavilla ldquoLista comentada de los anfibiosde ParaguayrdquoCuadernos deHerpetologıa vol 20 no 2 pp 3ndash792006
[26] I De La Riva J Kohler S Lotters and S Reichle ldquoTenyears of research on Bolivian amphibians updated checklistdistribution taxonomic problems literature and iconographyrdquoRevista Espanola Herpetologica vol 14 pp 19ndash164 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
12 Advances in Zoology
UFMT 11833 UFMT 11836 UFMT 11839 Goias Uruacu(14∘3110158403510158401015840S 49∘0710158405410158401015840W)-F UFMT 18397-400 UFMT18458-9 M UFMT 18401-15 UFMT 18458-64 Mato GrossoBarra do Garcas (15∘3110158405710158401015840S 52∘1410158401010158401015840W)-M UFMT11097 UFMT 11307 UFMT 11319 UFMT 11324 Caceres(16∘1710158405910158401015840S 58∘0910158400910158401015840W)-F UFMT 5906 UFMT 5950UFMT 5955 UFMT 5962 UFMT 9152 UFMT 10445UFMT 10448 UFMT 13669 M UFMT 10451-2 UFMT10455 UFMT 10458 UFMT 10466 UFMT 10495 UFMT10506 UFMT 10508 UFMT 13670 Chapada dos Guimaraes(type-locality 14∘5010158403410158401015840S 55∘2310158401010158401015840W)-F UFMT 8109 MUFMT 487 UFMT 817 UFMT 820 UFMT 12890 Cuiaba(15∘3910158403310158401015840S 55∘5610158403010158401015840W)-M UFMT 15980 UFMT 2426UFMT 2430 UFMT 2432 UFMT 2434-7 UFMT 2439UFMT 7399 UFMT 7653 UFMT 8177-8 UFMT 8180UFMT 8182 UFMT 8184-5 UFMT 13671 Nossa Senhorado Livramento (16∘2110158405810158401015840S 56∘1810158403310158401015840W)-F UFMT 18465UFMT 352 UFMT 6436 UFMT 6466-7 UFMT 6488UFMT 6511 M UFMT 4343 UFMT 6487 UFMT 6491UFMT6498UFMT6515Pocone (16∘3010158405810158401015840S 56∘4410158405310158401015840W)-M UFMT 348-50 UFMT 889 UFMT 4316 UFMT 4318UFMT 4321 UFMT 13672 and Porto Estrela (15∘3510158400510158401015840S57∘1310158402010158401015840W)-F UFMT 18466-7 UFMT 138 UFMT 13482M UFMT 18468-9 UFMT 402 UFMT 2200 UFMT 11346Sao Paulo Icem (20∘2010158403110158401015840S 49∘1110158404210158401015840W)-F UFMT 18421UFMT 18470-2 M UFMT 18422-3 UFMT 18473 and AltoAlegre (21∘3310158402010158401015840S 50∘1310158402210158401015840W)-F UFMT 18474-5 UFMT18479 MUFMT 18476-8 UFMT 18480-6
Pseudopaludicola saltica Brazil Mato Grosso Chapadados Guimaraes (type-locality 15∘2310158400910158401015840S 55∘5010158402410158401015840W)-MUFMT 482 UFMT 819 UFMT 821 UFMT 823 UFMT 1433-5 UFMT 1437-41 UFMT 2873 UFMT 2877 UFMT 2880-1F UFMT 1442 Cuiaba M UFMT 270 UFMT 473 UFMT476 UFMT 13657-68 F UFMT 13655-6) Nova Lacerda (MUFMT 13499-501) Porto Estrela Estacao Ecologica da Serradas Araras (M UFMT 561) and Vila Bela da SantıssimaTrindade (M UFMT 4082 UFMT 4112 UFMT 4123 UFMT4147 UFMT4153 UFMT4157 UFMT4172)MatoGrosso doSul Sonora (M UFMT 1147 UFMT 1195)
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho (type-locality 20∘0610158403210158401015840S 43∘5810158405310158401015840W)-F MCNAM 3675 MUFMT 18424 UFMT 18451 MCNAM 3677-8 MCNAM3680 Itabirito (20∘1310158402910158401015840S 43∘4810158404910158401015840W)-F MCNAM14620-1 M MCNAM 14625 Lavras Novas (20∘2810158405710158401015840S43∘3010158405210158401015840W)-F MCNAM 3694 M MCNAM 3695MCNAM 3690 Mariana (20∘0910158401210158401015840S 43∘3010158400210158401015840W)-FMCNAM 6465 M MCNAM 6457 MCNAM 6461-2 OuroBranco (20∘3010158401610158401015840S 43∘4210158400410158401015840W)-M MCNAM 6559 SaoJoao Del Rei (21∘0810158402510158401015840S 44∘1710158403110158401015840W)-M UFMT 18425-6UFMT 18452-3 and Botumirim (16∘4410158401310158401015840S 42∘3410158402910158401015840W)-FMCNAM 6713 M MCNAM 6832 MCNAM 6834 MCNAM6636 MCNAM 6642-3
B Analyzed Sound Files
Pseudopaludicola murundu Brazil Sao Paulo Rio Claro(type-locality) LH 676 no voucher specimen LH 677 call
fromUFMT 18455 LH 678 call fromUFMT 18395 and FNJV12976 no voucher specimen Minas Gerais Sao Roque deMinas (20∘1310158402010158401015840S 46∘2710158402410158401015840W) FNJV 4575 no voucherspecimen and Pocos de Caldas (21∘5510158400410158401015840S 46∘3410158400210158401015840W)FNJV 4576 no voucher specimen
Pseudopaludicola mystacalis Brazil Ceara Itapipoca(03∘2410158405810158401015840S 39∘4110158403110158401015840W) LH 655 no voucher specimenTaiba (03∘2510158404410158401015840S 38∘5710158404310158401015840W) LH 658 no voucher spec-imen Goias Uruacu LH 639 call from UFMT 18410) MatoGrosso Chapada dos Guimaraes (type-locality) LH 13A-05no voucher specimen) Caceres LH 47A-04 call fromUFMT10451 Cuiaba LH 14A-01 call from UFMT 2426 LH 14A-02 call from UFMT 2424 Pocone LH 01A-01 call fromUFMT 4321 and Nossa Senhora do Livramento LH 04A-10 call from UFMT 4330 Maranhao Balsa (07∘2810158404910158401015840S46∘0310158401910158401015840W) LH 284 no voucher specimen Piauı Brejo doPiauı (08∘1110158405010158401015840S 42∘4910158405910158401015840W) LH 184 call from UFMT11202 Para Primavera LH 352 call from UFMT 11836 SaoPaulo Icem LH 701 call from UFMT 18423
Pseudopaludicola saltica BrazilMatoGrossoCuiaba LH13A-01 call fromUFMT 8187Nova Lacerda LH 42A-06 callfrom UFMT 13499 LH 42A-07 call from UFMT 13500 andPorto Estrela LH 12 no voucher specimen LH 13 call fromUFMT 13678 LH 14 call fromUFMT 16423 LH 16 call fromUFMT 16417 LH 17 call from UFMT 16414 and LH 18 callfrom UFMT 16385 Minas Gerais Uberlandia (18∘5810158403010158401015840S48∘1710158402610158401015840W) LH 709 no voucher specimen
Pseudopaludicola serrana (junior synonym of Pmurundu) Brazil Minas Gerais Brumadinho LH 673call from UFMT 18451 LH 674 no voucher specimen andSao Joao Del Rei LH 675 call from UFMT 18426 and FNJV12879-80 no voucher specimen
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
Acknowledgments
Special thanks go to Felipe Franco Curcio Diva MariaBorges-Nojosa and Luciana Barreto Nascimento for allow-ing access to the material under their care at ldquoColecaoZoologica de Vertebrados da Universidade Federal de MatoGrossordquo (UFMT) ldquoColecao Herpetologica da UniversidadeFederal do Cearardquo (UFC) and ldquoMuseu de Ciencias Naturaisrdquo(MCNAM Belo Horizonte Minas Gerais) respectively toAdao J Cardoso (in memoriam) and Luis F Toledo for therecordings and for allowing access respectively to bioa-coustic samples deposited at ldquoFonoteca Neotropical JacquesVielliardrdquo (FNJV) to the CNPq project ldquoRede de pesquisa emanfıbios e repteis de ecossistemas nao florestais brasileirosrdquo(Process no 5633522010-8) for logistical support to VivianUhlig (RANICMBio) for estimates of extent of occurrenceAndre Pansonato thanks ldquoCoordenacao de Aperfeicoamentode Pessoal de Nivel Superiorrdquo (CAPES) for a PhD scholar-ship and Christine Strussmann thanks CNPq for a researchfellowship (Process no 3095412012-3)
Advances in Zoology 13
References
[1] K D Wells The Ecology amp Behavior of Amphibians TheUniversity of Chicago Chicago Ill USA 2007
[2] M Vences M Gehara J Kohler and F Glaw ldquoDescription of anewMalagasy treefrog (Boophis) occurring syntopically with itssister species and a plea for studies on non-allopatric speciationin tropical amphibiansrdquo Amphibia Reptilia vol 33 no 3-4 pp503ndash520 2012
[3] I De La Riva R Marquez and J Bosch ldquoDescription ofthe advertisement calls of some South American Hylidae(Amphibia Anura) taxonomic and methodological conse-quencesrdquo Bonner Zoologische Beitrage vol 47 pp 175ndash185 1997
[4] F S de Andrade and T R de Carvalho ldquoA new species of Pseu-dopaludicola Miranda-Ribeiro (Leiuperinae LeptodactylidaeAnura) from the Cerrado of southeastern Brazilrdquo Zootaxa vol3608 no 5 pp 389ndash397 2013
[5] D Cardozo and L F Toledo ldquoTaxonomic status of Pseudopalu-dicola riopiedadensis Mercadal de Barrio and Barrio 1994(Anura Leptodactylidae Leiuperinae)rdquo Zootaxa vol 3734 pp571ndash582 2013
[6] T R de Carvalho ldquoA new species of PseudopaludicolaMiranda-Ribeiro (Leiuperinae Leptodactylidae Anura) from the Cer-rado of southeastern Brazil with a distinctive advertisement callpatternrdquo Zootaxa no 3328 pp 47ndash54 2012
[7] F M Magalhaes D Loebmann M N C Kokubum C F BHaddad and A A Garda ldquoA new species of Pseudopaludi-cola (Anura Leptodactylidae Leiuperinae) from NortheasternBrazilrdquo Herpetologica vol 70 pp 77ndash88 2014
[8] A Pansonato C Strussmann J R Mudrek and I A Mar-tins ldquoMorphometric and bioacoustic data on three species ofPseudopaludicola Miranda-Ribeiro 1926 (Anura Leptodactyl-idae Leiuperinae) described from Chapada dos GuimaraesMato Grosso Brazil with the revalidation of Pseudopaludicolaameghini (Cope 1887)rdquo Zootaxa vol 3620 no 1 pp 147ndash1622013
[9] I J Roberto D Cardozo and R W Avila ldquoA new speciesof Pseudopaludicola (Anura Leiuperidae) from Western PiauıState Northeast Brazilrdquo Zootaxa vol 3636 no 2 pp 348ndash3602013
[10] S B Barreto M S Tinoco D Couto-Ferreira and H CBrowne-Ribeiro ldquoDistribuicao de Pseudopaludicola aff falcipes(Anura Leiuperidae) na restinga do litoral norte da BahiaBrasilrdquoRevista Latino-Americana de Conservacao vol 2 pp 27ndash36 2012
[11] E R Favero A C P Veiga-Menoncello D C Rossa-Feres et alldquoIntrageneric karyotypic variation in Pseudopaludicola (AnuraLeiuperidae) and its taxonomic relatednessrdquo Zoological Studiesvol 50 no 6 pp 826ndash836 2011
[12] M Jansen R Bloch A Schulze andM Pfenninger ldquoIntegrativeinventory of Boliviarsquos lowland anurans reveals hidden diversityrdquoZoologica Scripta vol 40 no 6 pp 567ndash583 2011
[13] C P D Prado M Uetanabaro and C F B Haddad ldquoBreed-ing activity patterns reproductive modes and habitat use byanurans (Amphibia) in a seasonal environment in the PantanalBrazilrdquo Amphibia Reptilia vol 26 no 2 pp 211ndash221 2005
[14] R A Silva I A Martins and D C Rossa-Feres ldquoBioacustica esıtio de vocalizacao em taxocenoses de anfıbios de area abertano Noroeste Paulistardquo Biota Neotropica vol 8 pp 123ndash1342008
[15] L F Toledo ldquoDescription of a new species of PseudopaludicolaMiranda-Ribeiro 1926 from the state of Sao Paulo SoutheasternBrazil (Anura Leiuperidae)rdquoZootaxa no 2681 pp 47ndash56 2010
[16] L F Toledo S Siqueira T CDuarte A C P Veiga-MenoncelloS M Recco-Pimentel and C F B Haddad ldquoDescription of anew species of Pseudopaludicola Miranda-Ribeiro 1926 fromthe state of Sao Paulo Southeastern Brazil (Anura Leiuperi-dae)rdquo Zootaxa no 2496 pp 38ndash48 2010
[17] C F B Haddad and A J Cardoso ldquoTaxonomia de tres especiesde Pseudopaludicola (Anura Leptodactylidae)rdquo Papeis Avulsosde Zoologia vol 36 pp 287ndash300 1987
[18] T C Duarte A C P Veiga-Menoncello J F R Lima et alldquoChromosome analysis in Pseudopaludicola (Anura Leiuperi-dae) with description of sex chromosomes XXXY in P salticardquoHereditas vol 147 no 2 pp 43ndash52 2010
[19] A C P Veiga-Menoncello L B Lourenco C Strussmannet al ldquoA phylogenetic analysis of Pseudopaludicola (Anura)providing evidence of progressive chromosome reductionrdquoZoologica Scripta vol 43 no 3 pp 261ndash272 2014
[20] W R Heyer A S Rand C A G Cruz O L Peixoto and CE Nelson ldquoFrogs of Boraceiardquo Arquivos de Zoologia vol 31 pp231ndash410 1990
[21] W E Duellman The Hylid Frogs of Middle America vol 1 ofMonograph of the Museum of Natural History of University ofKansas 1970
[22] R Development Core Team The R Project for Statistical Com-puting Vienna Austria 2013 httpwwwr-projectorg
[23] P E Vanzolini ldquoEcological and geographical distribution oflizards in Pernambuco Northeastern Brasil (Sauria)rdquo PapeisAvulsos de Zoologia vol 18 no 4 pp 61ndash90 1974
[24] J M Cei ldquoAmphibians of Argentinardquo Monitore ZoologicoItaliano Nuova Serie Monografia vol 2 pp 1ndash609 1980
[25] F Brusquetti and E O Lavilla ldquoLista comentada de los anfibiosde ParaguayrdquoCuadernos deHerpetologıa vol 20 no 2 pp 3ndash792006
[26] I De La Riva J Kohler S Lotters and S Reichle ldquoTenyears of research on Bolivian amphibians updated checklistdistribution taxonomic problems literature and iconographyrdquoRevista Espanola Herpetologica vol 14 pp 19ndash164 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
Advances in Zoology 13
References
[1] K D Wells The Ecology amp Behavior of Amphibians TheUniversity of Chicago Chicago Ill USA 2007
[2] M Vences M Gehara J Kohler and F Glaw ldquoDescription of anewMalagasy treefrog (Boophis) occurring syntopically with itssister species and a plea for studies on non-allopatric speciationin tropical amphibiansrdquo Amphibia Reptilia vol 33 no 3-4 pp503ndash520 2012
[3] I De La Riva R Marquez and J Bosch ldquoDescription ofthe advertisement calls of some South American Hylidae(Amphibia Anura) taxonomic and methodological conse-quencesrdquo Bonner Zoologische Beitrage vol 47 pp 175ndash185 1997
[4] F S de Andrade and T R de Carvalho ldquoA new species of Pseu-dopaludicola Miranda-Ribeiro (Leiuperinae LeptodactylidaeAnura) from the Cerrado of southeastern Brazilrdquo Zootaxa vol3608 no 5 pp 389ndash397 2013
[5] D Cardozo and L F Toledo ldquoTaxonomic status of Pseudopalu-dicola riopiedadensis Mercadal de Barrio and Barrio 1994(Anura Leptodactylidae Leiuperinae)rdquo Zootaxa vol 3734 pp571ndash582 2013
[6] T R de Carvalho ldquoA new species of PseudopaludicolaMiranda-Ribeiro (Leiuperinae Leptodactylidae Anura) from the Cer-rado of southeastern Brazil with a distinctive advertisement callpatternrdquo Zootaxa no 3328 pp 47ndash54 2012
[7] F M Magalhaes D Loebmann M N C Kokubum C F BHaddad and A A Garda ldquoA new species of Pseudopaludi-cola (Anura Leptodactylidae Leiuperinae) from NortheasternBrazilrdquo Herpetologica vol 70 pp 77ndash88 2014
[8] A Pansonato C Strussmann J R Mudrek and I A Mar-tins ldquoMorphometric and bioacoustic data on three species ofPseudopaludicola Miranda-Ribeiro 1926 (Anura Leptodactyl-idae Leiuperinae) described from Chapada dos GuimaraesMato Grosso Brazil with the revalidation of Pseudopaludicolaameghini (Cope 1887)rdquo Zootaxa vol 3620 no 1 pp 147ndash1622013
[9] I J Roberto D Cardozo and R W Avila ldquoA new speciesof Pseudopaludicola (Anura Leiuperidae) from Western PiauıState Northeast Brazilrdquo Zootaxa vol 3636 no 2 pp 348ndash3602013
[10] S B Barreto M S Tinoco D Couto-Ferreira and H CBrowne-Ribeiro ldquoDistribuicao de Pseudopaludicola aff falcipes(Anura Leiuperidae) na restinga do litoral norte da BahiaBrasilrdquoRevista Latino-Americana de Conservacao vol 2 pp 27ndash36 2012
[11] E R Favero A C P Veiga-Menoncello D C Rossa-Feres et alldquoIntrageneric karyotypic variation in Pseudopaludicola (AnuraLeiuperidae) and its taxonomic relatednessrdquo Zoological Studiesvol 50 no 6 pp 826ndash836 2011
[12] M Jansen R Bloch A Schulze andM Pfenninger ldquoIntegrativeinventory of Boliviarsquos lowland anurans reveals hidden diversityrdquoZoologica Scripta vol 40 no 6 pp 567ndash583 2011
[13] C P D Prado M Uetanabaro and C F B Haddad ldquoBreed-ing activity patterns reproductive modes and habitat use byanurans (Amphibia) in a seasonal environment in the PantanalBrazilrdquo Amphibia Reptilia vol 26 no 2 pp 211ndash221 2005
[14] R A Silva I A Martins and D C Rossa-Feres ldquoBioacustica esıtio de vocalizacao em taxocenoses de anfıbios de area abertano Noroeste Paulistardquo Biota Neotropica vol 8 pp 123ndash1342008
[15] L F Toledo ldquoDescription of a new species of PseudopaludicolaMiranda-Ribeiro 1926 from the state of Sao Paulo SoutheasternBrazil (Anura Leiuperidae)rdquoZootaxa no 2681 pp 47ndash56 2010
[16] L F Toledo S Siqueira T CDuarte A C P Veiga-MenoncelloS M Recco-Pimentel and C F B Haddad ldquoDescription of anew species of Pseudopaludicola Miranda-Ribeiro 1926 fromthe state of Sao Paulo Southeastern Brazil (Anura Leiuperi-dae)rdquo Zootaxa no 2496 pp 38ndash48 2010
[17] C F B Haddad and A J Cardoso ldquoTaxonomia de tres especiesde Pseudopaludicola (Anura Leptodactylidae)rdquo Papeis Avulsosde Zoologia vol 36 pp 287ndash300 1987
[18] T C Duarte A C P Veiga-Menoncello J F R Lima et alldquoChromosome analysis in Pseudopaludicola (Anura Leiuperi-dae) with description of sex chromosomes XXXY in P salticardquoHereditas vol 147 no 2 pp 43ndash52 2010
[19] A C P Veiga-Menoncello L B Lourenco C Strussmannet al ldquoA phylogenetic analysis of Pseudopaludicola (Anura)providing evidence of progressive chromosome reductionrdquoZoologica Scripta vol 43 no 3 pp 261ndash272 2014
[20] W R Heyer A S Rand C A G Cruz O L Peixoto and CE Nelson ldquoFrogs of Boraceiardquo Arquivos de Zoologia vol 31 pp231ndash410 1990
[21] W E Duellman The Hylid Frogs of Middle America vol 1 ofMonograph of the Museum of Natural History of University ofKansas 1970
[22] R Development Core Team The R Project for Statistical Com-puting Vienna Austria 2013 httpwwwr-projectorg
[23] P E Vanzolini ldquoEcological and geographical distribution oflizards in Pernambuco Northeastern Brasil (Sauria)rdquo PapeisAvulsos de Zoologia vol 18 no 4 pp 61ndash90 1974
[24] J M Cei ldquoAmphibians of Argentinardquo Monitore ZoologicoItaliano Nuova Serie Monografia vol 2 pp 1ndash609 1980
[25] F Brusquetti and E O Lavilla ldquoLista comentada de los anfibiosde ParaguayrdquoCuadernos deHerpetologıa vol 20 no 2 pp 3ndash792006
[26] I De La Riva J Kohler S Lotters and S Reichle ldquoTenyears of research on Bolivian amphibians updated checklistdistribution taxonomic problems literature and iconographyrdquoRevista Espanola Herpetologica vol 14 pp 19ndash164 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
