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Morphological and Karyotypic Contributions for a Better Taxonomic Definition of the Frog Ischnocnema Ramagii (Boulenger, 1888) (Anura, Brachycephalidae)

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Morphological and Karyotypic Contributions for a Better Taxonomic Definition of the Frog Ischnocnema Ramagii (Boulenger, 1888) (Anura, Brachycephalidae) South American Journal of Herpetology, 4(2), 2009, 164-172 © 2009 Brazilian Society of Herpetology MORPHOLOGICAL AND KARYOTYPIC CONTRIBUTIONS FOR A BETTER TAXONOMIC DEFINITION OF THE FROG ISCHNOCNEMA RAMAGII (BOULENGER, 1888) (ANURA, BRACHYCEPHALIDAE) MARCELO F. NAPOLI1,4, FERNANDO ANANIAS2, PATRICIA M. FONSECA1, AND ANA PAULA Z. SILVA3 1 Museu de Zoologia, Departamento de Zoologia, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão de Jeremoabo, Ondina, 40170‑115, Salvador, BA, Brasil. E‑mail: [email protected], [email protected] 2 Curso de Ciências Biológicas, Universidade São Francisco (USF), Avenida São Francisco de Assis, 218, Jardim São José, 12916‑900, Bragança Paulista, SP, Brasil. E‑mail: [email protected] 3 Laboratório Especial de Ecologia e Evolução, Instituto Butantan, Avenida Vital Brasil, 1500, 05503‑900, São Paulo, SP, Brasil. E‑mail: [email protected] 4 Corresponding author. ABSTRACT. In this study we describe the morphological variation of Ischnocnema ramagii from a population sample within the Municipality of Salvador, Bahia State, Brazil, and characterize two extremely distinct morphotypes within this taxon (striped vs. non-striped dorsum); we describe its karyotype, and compare the karyotypic structure of the distinct morphotypes recognized herein. Specimens with striped dorsa were less common (13-18%) than those with non-striped dorsa (81-86%), the latter group comprising a mix of discrete color pattern states, whose frequencies were not different among juveniles, males, and females. The PCAs on morphometric data resulted in a strong degree of superposition between striped and non-striped dorsa, for both genders. We encountered a diploid number of 30 chromosomes for both males and females, with chromosome pairs 1 to 15 being telocentric. The karyotypic comparison between specimens with striped and non-striped dorsa did not show any noticeable difference. Nevertheless the karyotype of I. ramagii from Salvador, Bahia, differed from the karyotype described for I. paulodutrai from Ilhéus, Bahia, which showed a submetacentric chromosome pair. This result supports the presence of two full “sibling” species in Bahia State, one from the south (I. paulodutrai) and another from the north (I. ramagii), validating the identity of I. paulodutrai as a full species, and refuting the recognition of Salvador samples as I. paulodutrai. The high number of telocentric chromosomes suggests a closer relationship between I. ramagii and “Eleutherodactylinae” species from Central America and the northern region of Brazil. KEYWORDS. Ischnocnema paulodutrai, Intra-population variation, Karyotype, Polymorphism, Size and shape variation. INTRODUCTION I. paulodutrai; (3) possible morphological polymor- phism within populations; and (4) complex variation The “Eleutherodactylinae” frog Ischnocnema ra‑ of advertisement calls within and among geographic magii (Boulenger, 1888) (sensu Heinicke et al., 2007) populations. The current poor knowledge of local inhabits Tropical Atlantic forests of northeastern Bra- and geographic variation of both species prevents an zil, from Paraíba State to Bahia State (Frost, 2008). accurate assignment of a specimen to a given taxa, The species I. ramagii was described as Hylodes which is usually done by taking into account the geo- ramagii, based on a single specimen collected by graphic distance between the area of collection and G. A. Ramage in the Municipality of Igarassu, State the respective type-localities (I. paulodutrai, Ilhéus, of Pernambuco, northeastern Brazil. In the last few southern Bahia State, 14°47’S, 39°02’W; I. rama‑ years, similar morphotypes have been registered from gii, Igarassu, Pernambuco State, 07°50’S, 34°54’W; the State of Bahia, Brazil, usually being recognized ca. 890 km distance from each other). Because of as I. ramagii (e.g., Munduruca, 2005; Juncá, 2006; the above statements, we did not follow Napoli and Bastazini et al., 2007) or I. paulodutrai (Bokermann, Brandão (2003) in allocating specimens from Salva- 1975) (e.g., Napoli and Brandão, 2003). Other closely dor to I. paulodutrai. related morphotypes have been captured within the In this study, we make a first assessment to im- Tropical Atlantic Forest and Caatinga biomes by us prove the morphologic and cytogenetic knowledge of and by other researchers during surveys of anurans, I. ramagii, using population samples from a patch of but probably belong to species not yet described Atlantic Forest remnant located in the campus of the (pers. obs.). Universidade Federal da Bahia (UFBA), at a neigh- Concerning the correct identification of specimens borhood named Ondina, in the Municipality of Sal- of Ischnocnema ramagii and I. paulodutrai, four ma- vador, Bahia State, Brazil. We decided to limit our jor problems can be postulated: (1) the short original analysis to this local population for three reasons: description of I. ramagii; (2) the poor diagnosis of (1) only one type of advertisement call is found in Napoli, M. F. et al. 165 this population, which led us to assume that only one collections (acronyms in parenthesis): Comissão Ex- species occurs at the locality; (2) this local population ecutiva do Plano de Cultivo da Lavoura Cacaueira, contains two extremely distinct morphotypes, distin- Municipality of Ilhéus, Bahia State (CEPLAC); Cé- guished by the presence or not of longitudinal brown lio Haddad Collection (CFBH), deposited in the De- stripes on the dorsum, which makes their descriptions partamento de Zoologia, Instituto de Biociências, very important for an accurate definition of species Universidade Estadual Paulista, Municipality of Rio limits; (3) there is no doubt about the conspecific- Claro, São Paulo State; Museu de Zoologia, Univer- ity of these morphotypes, as we obtained 13 frogs of sidade Federal da Bahia, Municipality of Salvador, both (UFBA 2914; 54% striped dorsum; 46% non- Bahia State (UFBA). striped dorsum) within a single clutch of large-yolked We analyzed 151 specimens of Ischnocnema ra‑ terrestrial eggs; and (4) many specimens are available magii (89 males, 22 females, and 40 juveniles) from from this locality (n = 151). a patch of Atlantic Forest remnant located in the cam- The goals of the present study are to (1) charac- pus of the Universidade Federal da Bahia, at a neigh- terize the morphological variation of Ischnocnema borhood named Ondina, in the Municipality of Salva- ramagii from a population sample within the Munici- dor, Bahia State, Brazil (12°59’S; 38°27’W). pality of Salvador, Bahia State, Brazil; (2) describe We developed outline drawings as a standard the karyotype; (3) assess the level of karyotypic poly- series for color patterns of dorsum, interocular bar, morphisms in the population; and (4) compare the post-orbital region, and sacral surface, recorded for karyotype of I. ramagii with the karyotype of I. pau‑ each specimen examined. When a new pattern was lodutrai from Ilhéus, Bahia State, by Siqueira et al. encountered, it was added to the standards. We fol- (2008). lowed Heyer (1984) as several aspects of the dorsal pattern are inherited independently in some species of Terrarana (Goin, 1950, 1960). The purpose of MATERIAL AND METHODS this procedure was to analyze (1) variation within this population and (2) differences among juveniles, Specimens used for descriptions or examined for males, and females. Drawings were made using a comparisons are deposited in the following Brazilian Leica MZ6 stereomicroscope with a drawing tube. FIGURE 1. Dorsal views of Ischnocnema ramagii from the Municipality of Salvador, Bahia State, Brazil. A, adult female with striped dor- sum, UFBA 3158, SVL 25.0 mm; B, adult female with non-striped dorsum, UFBA 2271, SVL 25.5 mm. Photographs by Rafael O. Abreu. 166 Morphology and Karyotype of Ischnocnema ramagii Chi-square analyses were performed to test whether measurements followed Heyer et al. (1990): UAR patterns observed differed in occurrence among juve- (upper arm), FAR (forearm), HAL (hand length). The niles, males, and females. The α-level of significance remaining measurements are LF1 (length of finger I) (P ≤ 0.05) was Bonferroni corrected (Bland, 2004). and LF2 (length of finger II), both as the straight line We measured 20 morphometric characters from 89 distance between the lower and upper borders of the adult males and 22 adult females of I. ramagii, which finger. We measured SVL, HL, HW, ITD, THL, TL, were recorded in millimeters. Fifteen measurements FL, UAR, FAR, and HAL with a vernier caliper, and followed Napoli (2005): SVL (snout-vent length), HL used an ocular micrometer in an SZ Olympus stereo- (head length), HW (head width), ED (eye diameter), microscope for the remaining variables. UEW (upper eyelid width), IOD (interorbital dis- We used the principal component analysis (PCA) tance), IND (internarial distance), END (eye-nostril to study multivariate patterns of shape and size varia- distance), NSD (nostril to tip of snout distance), TD tion. The first principal component (PC1) typically (tympanum diameter), THL (thigh length), TL (tibia expresses “size” variation when it has loadings of the length), FL (foot length), 3FD (third finger disk di- same magnitude and sign for all growth-dependent ameter), and 4TD (fourth toe disk diameter). Three variables (Humphries et al., 1981). The remaining FIGURE 2. Standards for color patterns of (A) dorsum, (B) interocular bar, (C) post-orbital region, and (D) sacral surface. Additional stan- dards not figured are: A1, B1, C1, and D1, which
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