The advertisement call, color patterns and distribution of Ischnocnema izecksohni (Caramaschi and Kisteumacher, 1989) (Anura, Brachycephalidae)

The advertisement call, color patterns and distribution of Ischnocnema izecksohni (Caramaschi and Kisteumacher, 1989) (Anura, Brachycephalidae)

Pedro P. G. TaucceI, ^*; Felipe S. F. Leite^I; Patrícia S. Santos^I; Renato N. Feio^II; Paulo C. A. Garcia^I

^ILaboratório de Herpetologia, Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais. 31270-901, Belo Horizonte, MG, Brasil

^IIMuseu de Zoologia João Moojen, Departamento de Biologia Animal, Universidade Federal de Viçosa. 36570-000, Viçosa, MG, Brasil

ABSTRACT

Ischnocnema izecksohni inhabits the gallery forests from the Quadrilátero Ferrífero, Southern Espinhaço range, state of Minas Gerais, southeastern Brazil, and it is considered endemic to this region. Its closest related species is I. nasuta according to the original description. We describe the advertisement call of I. izecksohni based on specimens recorded and collected at the municipality of Nova Lima, state of Minas Gerais, distant about 10 km straight line from its type locality. The advertisement call consists of a group of notes emitted sporadically without a regular interval between the calls. Call duration (n = 36 calls in four individuals) ranged from 1.03 to 1.85 s (= 1.52 ± 0.21 s) and the call rise time from 0.66 to 1.52 s (= 1.16 ± 0.25 s), with 34-57 notes per call (= 47.42 ± 6.03). Peak frequency ranged from 2250 to 2625 Hz, the dominant frequency from 1317.8 to 3128.0 Hz and interval between notes from 22.00 to 41.00 ms (= 28.63 ± 0.03 ms). From the examination of herpetological collections, morphological and bioacoustical data we extended the species known distribution ca. 200 km eastward, to ten new localities, all of them outside the Quadrilátero Ferrífero region, at the Mantiqueira mountain range. We analyzed color patterns and we find some dorsal patterns not described at the original description of I. izecksohni. We also make some comments concerning the taxonomic status of I. izecksohni and I. nasuta.

Key-words: Vocalization; Taxonomy; Polymorphism; Ischnocnema guentheri species series.

RESUMO

Ischnocnema izecksohni habita as matas de galeria do Quadrilátero Ferrífero, sul da Cadeia do Espinhaço, estado de Minas Gerais, sudeste do Brasil e é considerada endêmica desta região. Sua espécie mais próxima, de acordo com a descrição original, é I. nasuta. Descreve-se o canto de I. izecksohni baseado em espécimes gravados e coletados em Nova Lima, MG, que dista 10 km em linha reta da localidade tipo da espécie. O canto de anúncio consiste em um grupo de notas emitidas esporadicamente sem um intervalo regular entre os cantos. A duração do canto (n = 36 cantos em quatro indivíduos) variou de 1,03 até 1,85 s (= 1,52 ± 0,21 s) e o tempo até a amplitude máxima do canto de 0,66 to 1,52 s (= 1,16 ± 0,25 s), com 34-57 notas por canto (= 47.42 ± 6.03). A freqüência de pico variou de 2250 a 2625 Hz, a freqüência dominante de 1317,8 a 3128,0 Hz e o intervalo entre as notas de 22,00 to 41,00 ms (= 28,63 ± 0,03 ms). A partir do exame de coleções herpetológicas, dados morfológicos e bioacústicos estendeu-se a distribuição da espécie para cerca de 200 km a leste, para mais dez localidades, todas elas fora do Quadrilátero Ferrífero, no complexo da Mantiqueira. Foram analisados padrões de coloração e alguns padrões dorsais além daquele presente na descrição original foram encontrados. São feitos comentários acerca do status taxonômico de I. izecksohni e I. nasuta.

Palavras-chave: Vocalização; Taxonomia; Polimorfismo; Série de Ischnocnema guentheri.

INTRODUCTION

The genus Ischnocnema Reinhardt & Lütken was recently revalidated to include the old eleutherodactylid frogs from the Brazilian Atlantic Forest (Heinicke et al., 2007), except Haddadus binotatus (Spix, 1824) and H. plicifer (Boulenger, 1888), allocated in the family Craugastoridae Hedges, Duellman & Heinicke, 2008. Ischnocnema contains 34 species split in the I. guentheri, I. lactea, I. parva, I. ramagii and I. verrucosa species series (Hedges et al. 2008; Frost, 2011). The I. guentheri species series comprises eleven species: I. epipeda (Heyer, 1984), I. erythromera (Heyer, 1984), I. gualteri (B. Lutz, 1974), I. guentheri (Steindachner, 1864), I. henselii (Peters, 1870), I. hoehnei (A. Lutz, 1958), I. izecksohni (Caramaschi & Kisteumacher, 1989), I. nasuta (A. Lutz, 1925), I. octavioi (Bokermann, 1965), I. oea (Heyer, 1984), and I. vinhai (Bokermann, 1975). This species series is widely distributed throughout the Atlantic Forest biome occurring since the southern state of Bahia to the state of Santa Catarina, and I. henselli occurs at the Araucaria forests in the state of Rio Grande do Sul, Brazil, and Misiones, Argentina (Hedges et al. 2008).

Ischnocnema izecksohni inhabits the gallery forests from the Quadrilátero Ferrífero, Southern Espinhaço range, state of Minas Gerais, southeastern Brazil, and it is considered endemic to this region (Leite et al. 2008). The species is described from Parque das Mangabeiras, Municipality of Belo Horizonte (19°55'S and 43°56'W, approximately 850 m elevation) and the description is based on three specimens (two adult females and an adult male), and its closest related species is I. nasuta according to the original description. Ischnocnema izecksohni differs from I. nasuta because it is slightly more robust, has smaller tympanum, shorter snout, more developed fringes on toes, and different coloration (Caramaschi & Kisteumacher, 1989). Within the series of I. guentheri, only four species have their vocalization described: I. nasuta, based on a specimen from Parque Nacional do Caparaó, state of Minas Gerais, southeastern Brazil; I. gualteri, based on a specimen from the type locality (municipality of Teresópolis, state of Rio de Janeiro, southeastern Brazil) and I. guentheri, based on a specimen recorded in the municipality of Pirabeiraba, Santa Catarina, at a distance about 670 km straight line from the type locality of the species (municipality of Rio de Janeiro, state of Rio de Janeiro) (Heyer, 1984). Heyer et al. (1990) describe the advertisement call of I. guentheri from Estação Biológica da Boracéia, municipality of Salesópolis, SP. Kwet & Solé (2005) revalidated I. henselii, and described two different vocalizations for the species. The authors describe and compare calls of some populations of I. guentheri, which leads them to conclude that I. guentheri comprises a complex of two or three species. The anuran advertisement call is considered species-specific and functions in mate recognition, and vocal differences are important pre-zygotic isolation mechanisms (Kelley et al. 2001). With the technology becoming increasingly affordable and easy to use, the bioacoustic parameters have become a taxonomic tool as important as morphological data in the anuran systematics. It helps untie species identity in taxonomically difficult and morphologically cryptic or polymorphic groups (Kwet & Angulo, 2002; Angulo et al. 2003; Angulo & Reichle, 2008; Channing et al. 2002; Ron et al. 2005; Toledo et al. 2007). Heyer (1984) separated some exemplars of I. guentheri species series in 14 dorsal patterns. All the species analyzed in the paper have more than one dorsal pattern. Caramaschi & Kisteumacher (1989) only describe one type of dorsal pattern for I. izecksohni, but this is probably due the few exemplars used in the description (2 females and a male). Herein we describe the advertisement call of I. izecksohni and we compare it to some reported and unreported calls of other populations within the I. guentheri species series. We also describe different color patterns and extend the geographic distribution for the species in Minas Gerais, Brazil.

MATERIALS AND METHODS

Four specimens of I. izecksohni were recorded at RPPN Mata Samuel de Paula, municipality of Nova Lima, in the Quadrilátero Ferrífero region, state of Minas Gerais, southeastern Brazil (20°00'S, 43°52'W, approximately 900 m elevation), approximately 10 km straight-line from the type locality. Two specimens were recorded at Parque Estadual da Serra do Brigadeiro (PESB), municipalities of Araponga and Fervedouro, state of Minas Gerais, in the Mantiqueira mountain range (20°43'S, 42°29'W, approximately 1300 m elevation), approximately 200 km straight-line from the type locality. Voucher specimens are deposited at the Coleção Herpetológica da Universidade Federal de Minas Gerais (UFMG) (^{Appendix I}). Records were made with a digital recorder Marantz PMD 660, with a frequency sampling rate of 16 bits, and a Sennheiser ME-66 super-cardioid shotgun condenser microphone and analyzed with the program Raven 1.4 beta for Windows (Cornell Lab of Ornithology Research Program Bioacoustics Workstation). The audiospectrograms were produced with FFT of 256 points, overlap 75% and window Hamming. Resolution, contrast and brightness settings were the program default. Measurements of the following acoustic parameters were taken: call duration, note interval, notes per call, according to Kwet & Solé (2005); call rise time follows Cocroft & Ryan (1995). Peak frequency was obtained directly from the software. Temporal parameters were measured in seconds (s) or milliseconds (ms) and spectral parameters in Hertz (Hz).

For the description of the color patterns and distribution extension we examined specimens (^{Appendix I}) from the Museu de Zoologia João Moojen, Universidade Federal de Viçosa (MZUFV), Viçosa, Minas Gerais, Brazil; the Coleção Herpetológica da Universidade Federal de Minas Gerais (UFMG) and the Museu de Ciências Naturais, Pontifícia Universidade Católica de Minas Gerais (MCNAM), both in Belo Horizonte, Minas Gerais, Brazil. Color patterns follow Heyer (1984), except for two new general dorsal patterns (Fig. 1) included here: A-8*, which is the variegated pattern with two dark spots in the back; and B-3, which is the same as Heyer's B-1 pattern but with just one dark spot in the back.

RESULTS AND DISCUSSION

Males were found calling at night inside gallery forests. Recorded individuals (UFMG0039, UFMG0040 and UFMG0041) were found on vegetation at a height ranging from 50 cm to about 2 m from the ground. The advertisement call consists of a group of notes emitted sporadically without a regular interval between the calls. Like the other species from the series (see Kwet & Solé, 2005 and Heyer, 1984), it increases energy over time until it reaches a peak. Call duration (n = 36 calls in four individuals) ranged from 1.03 to 1.85 s (mean = 1.52 ± 0.21 s) and the call rise time from 0.66 to 1.52 s (mean = 1.16 ± 0.25 s), with 34-57 notes per call (mean = 47.42 ± 6.03) (Fig. 2 and Table 1). Peak frequency varied from 2250 to 2625 Hz, the dominant frequency from 1317.8 to 3128.0 Hz and interval between notes from 22.00 to 41.00 ms (= 28.63 ± 0.03 ms).

The call of I. izecksohni differs from the call of I. gualteri and I. guentheri from the municipality of Pirabeiraba, state of Santa Catarina (Heyer, 1984), Boracéia and Bocaina, state of São Paulo, Morro do Baú, Guaramirim and Pirabeiraba, state of Santa Catarina (Kwet & Solé, 2005), because it has a larger number of notes per call. Regarding the call duration, I. izecksohni presents a shorter call than that of I. henselii (10.00 to 23.00 s) and I. guentheri from Morro do Baú (2.10 to 2.70 s). The advertisement call of I. izecksohni has the smallest interval between notes from all the calls analyzed by Kwet & Solé (2005). This parameter could not be compared to the calls in Heyer (1984), since it was not analyzed in the paper.

The calls from the municipality of Nova Lima are very similar to that from the PESB, and the two populations are definitively conspecific. One specimen from the PESB has the call with the largest duration (1.68-2.15 s), but this is probably due to population variations.

The call of Ischnocnema nasuta was described from Parque Nacional do Caparaó (PNC), state of Minas Gerais (Heyer, 1984), distant about 200 km straight line from the type locality of the species (municipality of Nova Friburgo, state of Rio de Janeiro). This call is really similar to I. izecksohni (table 1, fig. 1 and fig. 24 Heyer, 1984), suggesting that the two populations are conspecifics. We also examined some I. nasuta specimens provenient from PNC housed at Museu de Zoologia da Universidade de São Paulo (MZUSP), and the differences mentioned by Caramaschi & Kisteumacher (1989) do not apply to specimens examined. The taxonomic status of I. nasuta from PNC or even I. izecksohni in relation to I. nasuta is depending on the analysis of the call of I. nasuta from the type locality.

Literature data reports I. izecksohni for the municipalities of Belo Horizonte (Caramaschi & Kisteumacher, 1989), Nova lima (Nascimento et al. 1994), Ouro Preto (Pedralli et al. 2001), Rio Acima (Grandinetti & Jacobi, 2005), Catas Altas (Canelas & Bertoluci, 2007), São Gonçalo do Rio Abaixo (Bertoluci et al. 2009), Congonhas, and Ouro Branco (Leite et al. 2008), all of them at the Quadrilátero Ferrífero region. Based on recently collected and recorded specimens we report for the first time the occurrence of I. izecksohni for the PESB. The examination of herpetological collections allowed us to record the species also for the municipalities of Cataguases, Espera Feliz, Miraí, Muriaé, Patrocínio do Muriaé Pedra Dourada, Rio Preto, and Viçosa, at the Mantiqueira mountain range, state of Minas Gerais, outside the Quadrilátero Ferrífero, extending its distribution ca. 200 km eastward. We also collected specimens at the municipality of Simonésia, also at the Mantiqueira mountain range. Literature reports I. guentheri for the municipalities of Muriaé (Santana et al. 2010) and Ouro Branco (São-Pedro & Feio, 2010). We examined the vouchers from both localities and it corresponds to I. izecksohni. Silva et al. 2011 reported I. cf. izecksohni for the municipality of Viçosa based on vocalization records. It is probably I. izecksohni. For a complete distribution map see Fig. 3.

The general dorsal patterns observed were: A-1, A-4, A-5, A-6, A-8, A-8*, B-1 and B-3 (Fig. 1). The mid-dorsal pin stripe was absent or like A and E. The dorsolateral stripe was absent or like the A pattern. The snout pattern was mainly uniform, but we also observed A and B patterns. The interocular bar was absent or like B. The pelvic and supratympanic spots were mainly like A, but a few individuals showed the B pattern. Pelvic spots could be also absent in a few individuals. The loreal stripe was uniform or like A, B and C. The upper lip pattern was like A, B, C and D. The outer front aspect of the tibia was mainly like C, but the patterns A, B and uniform were also observed. The posterior surface of the thigh was A-1 for all the specimens analyzed. Detailed information about the patterns is showed in Table 2.

Caramaschi & Kisteumacher (1989) described the dorsal pattern of Ischnocnema izecksohni as "...variegated-mottled tan and a chevron-like mark on middle third of the body..." It looks like Heyer's A-1 pattern, but we have seen seven more dorsal patterns. They were not conclusive as a putative diagnosis for the species, as well as almost all the other color patterns. Heyer (1984) says that a boldly mottled posterior surface of the thigh pattern distinguishes I. nasuta from the other species of the I. guentheri species group and mostly I. guentheri individuals, which have a light area near the knee or uniform and indistinctly mottled posterior thigh patterns. All I. izecksohni specimens we analyzed have the same boldly mottled posterior surface of the thigh pattern as that of I. nasuta and we are not aware of any morphologic features distinguishing them. The diagnosis between the two species in Caramaschi & Kisteumacher (1989) is subjective.

As I. izecksohni and I. nasuta seems to be indistinguishable, two situations are possible. I. izecksohni occurs at the Espinhaço mountain range and at the Mantiqueira mountain range, and I. nasuta is a very close species occurring at Serra do Mar. Or, I. izecksohni and I. nasuta are the same species, with the first one being a junior synonym of the second one. Examination of both type series and the analysis of the call of I. nasuta from its type locality are necessary to make clear the taxonomic status of the two species, besides genetic and behavioral information.

ACKNOWLEDGEMENTS

We thank Luciana Nascimento (MCNAM) and Hussam Zaher (MZUSP) for the loan of specimens under their care. For support at MZUSP we thank Carolina Mello. Clarissa Canedo critically read the manuscript. C.F.B. Haddad granted access to Raven 1.4 beta. Paulo Pinheiro and Bruno Fehlberg (UFMG) gave fieldwork assistance. Instituto Estadual de Florestas (IEF) supported conducting field research at Parque Estadual Serra do Brigadeiro. Anglogold Ashanti supported conducting field research at RPPN Mata Samuel de Paula. Instituto Chico Mendes de Conservação da biodiversidade (ICMBio) gave collection permits. US Fish & Wildlife Service gave financial support. Paulo Garcia specially thanks Fapemig (Programa Pesquisador Mineiro) for financial support and CNPq for the productivity fellowship conceded.

Recebido em: 01.09.2011

Aceito em: 15.02.2012

Impresso em: 30.03.2012

Specimens Examined

MCNAM 509, 5215, 5216, 5573, 5574; MZUFV 1280, 1285, 1344, 2142, 4033, 6309-6312, 6787, 7083, 7106, 7107, 7112, 7393, 7394, 7564, 7565, 7632, 7688, 8022, 8730, 8884, 8926, 9043, 9765, 9766, 9951; MZUSP 57947, 133862, 135691; UFMG 0037-0041, 3286-3292.

• ANGULO, A. & REICHLE, S. 2008. Acoustic signals, species diagnosis, and species concepts: the case of a new cryptic species of Leptodactylus (Amphibia, Anura, Leptodactylidae) from the Chapare region, Bolivia. Zoological Journal of the Linnean Society, 152:59-77.
• Angulo, A.; Cocroft, R.B. & Reichle, S. 2003. Species identity in the genus Adenomera (Anura: Leptodactylidae) in Southeastern Peru. Herpetologica, 59:490-504.
• BERTOLUCI, J.; CANELAS, M.A.S.; EISEMBERG, C.C.; PALMUTI, C.F.S. & MONTIGELLI, G.G. 2009. Herpetofauna da Estação Ambiental de Peti, um fragmento de Mata Atlântica do estado de Minas Gerais, sudeste do Brasil. Biota Neotropica, 9:147-155.
• Canelas, M.A.S. & Bertoluci, J. 2007. Anurans of the Serra do Caraça, southeastern Brazil: species composition and phenological patterns of calling activity. Iheringia: Série Zoologia, 97:21-26.
• Caramaschi, U. & Kisteumacher, G. 1989. A new species of Eleutherodactylus (Anura: Leptodactylidae) from Minas Gerais, Southeastern Brazil. Herpetologica, 44:423-426.
• Channing, A.; Moyer, D. & Burger, M. 2002. Cryptic species of sharp-nosed reed frogs in the Hyperolius nasutus complex: advertisement call differences. African Zoology, 37:91-99.
• Cocroft, R.B. & Ryan, M.J. 1995. Patterns of advertisement call evolution in toads and chorus frogs. Animal Behaviour, 49, 283-303.
• Frost, D.R. 2011. Amphibian Species of the World 5.5, an Online Reference. Available at: http://research.amnh.org/vz/herpetology/amphibia Access in: 07/06/2011.
• GRANDINETTI, L. & JACOBI, C.M. 2005. Distribuição estacional e espacial de uma taxocenose de anuros (Amphibia) em uma área antropizada em Rio Acima, MG. Lundiana, 6:21-28.
• Hedges, S.B.; Duellman, W.E. & Heinicke, M.P. 2008. New World direct-developing frogs (Anura: Terrarana): Molecular phylogeny, classification, biogeography, and conservation. Zootaxa, 1737:1-182.
• Heinicke, M.P.; Duellman, W.E. & Hedges, S.B. 2007. Major Caribbean and Central American frog faunas originated by ancient oceanic dispersal. Proceedings of the National Academy of Sciences, 104:10092-10097.
• Heyer, W.R. 1984. Variation, systematics, and zoogeography of Eleutherodactylus guentheri and closely related species (Amphibia: Anura: Leptodactylidae). Smithsonian Contributions to Zoology, 402:1-42.
• Heyer, W.R.; Rand, A.S.; Cruz, C.A.G.; Peixoto, O.L. & Nelson, C.E. 1990. Frogs of Boracéia. Arquivos de Zoologia, 31:231-410.
• Kelley, D.B.; Tobias, M.L. & Horng, S. 2001. Producing and Perceiving Frog Songs: Dissecting the Neural Bases for Vocal Behaviors in Xenopus laevis. In: Ryan, M.J. (Ed.). Anuran Communication. Smithsonian Institution Press, Washington, U.S.A. p. 156-166.
• Kwet, A. & Angulo, A. 2002. A new species of Adenomera (Anura, Leptodactylidae) from the Araucaria Forest of Rio Grande do Sul (Brazil), with comments on the systematic status of southern populations of the genus. Alytes, 20:28-43.
• Kwet, A. & Solé, M. 2005. Validation of Hylodes henselii Peters, 1870, from Southern Brazil and description of acoustic variation in Eleutherodactylus guentheri (Anura: Leptodactylidae). Journal of Herpetology, 39:521-532.
• LEITE, F.S.F.; JUNCÁ, F.A. & ETEROVICK, P.C. 2008. Status do conhecimento, endemismo e conservação de anfíbios anuros da Cadeia do Espinhaço, Brasil. Megadiversidade, 4:158-176.
• Nascimento, L.B.; Miranda, A.C.L. & Balstaedt, T.A.M. 1994. Distribuição estacional e ocupação ambiental dos anfíbios anuros da área de proteção da captação da Mutuca (Nova Lima, MG). Bios, Cadernos do Departamento de Ciências Biológicas da PUC-MG, 2:5-12.
• Pedralli, G.; Neto, A.S.G. & Teixeira, M.C.B. 2001. Diversidade de anfíbios na região de Ouro Preto. Ciência Hoje, 178:70-73.
• RON, S.R., COLOMA, L.A. & CANNATELLA, D.C. 2005. A new cryptic species of Physalaemus (Anura: Leptodactylidae) from western Ecuador with comments on the call structure of the P. pustulosus species group. Herpetologica, 61:178-198.
• SANTANA, D.J.; SÃO-PEDRO, V.A.; HOTE, P.S.; ROBERTI, H.M.; SANT'ANNA, A.C.; FIGUEIREDO-DE-ANDRADE, C.A.; FEIO, R.N. 2010. Anurans in the region of the High Muriaé River, state of Minas Gerais, Brazil. Herpetology Notes, 3:1-10.
• SÃO-PEDRO, V.A. & FEIO, R.N. 2010. Distribuição espacial e sazonal de anuros em três ambientes na Serra do Ouro Branco, extremo sul da Cadeia do Espinhaço, Minas Gerais, Brasil. Biotemas, 23:143-154.
• Silva, E.T.; Ribeiro Filho, O.P. & Feio, R.N. 2011. Predation of Native Anurans by invasive bullfrogs in southeastern Brazil: spatial variation and effect of microhabitat use by prey. South American Journal of Herpetology, 6:1-10.
• TOLEDO, L.F.; GARCIA, P.C.A.; LINGNAU, R. & HADDAD, C.F.B. 2007. A new species of Sphaenorhynchus (Anura; Hylidae) from Brazil. Zootaxa, 1658:57-68.

APPENDIX I 

Publication Dates

• Publication in this collection
  02 Apr 2012
• Date of issue
  2012

History

• Received
  01 Sept 2011
• Accepted
  15 Feb 2012