Patrícia de Menezes Gondim 1,3*, Maria Juliana Borges-Leite 1,3, Luan Tavares Pinheiro 3, Diva Maria Borges-Nojosa 1,3 and Paulo Cascon 1,2

Transcrição

1 Herpetology Notes, volume 6: (2013) (published online on 23 August 2013) Microhabitat use (vertical distribution) by a population of Dendropsophus gr. microcephalus (Anura, Hylidae) in a forested area of coastal tableland of north-eastern Brazil Patrícia de Menezes Gondim 1,3*, Maria Juliana Borges-Leite 1,3, Luan Tavares Pinheiro 3, Diva Maria Borges-Nojosa 1,3 and Paulo Cascon 1,2 Abstract. In this work, we studied the vertical stratification of Dendropsophus gr. microcephalus in a coastal area of semievergreen forest board of north-eastern Brazil. We analysed sex, ontogenetic and seasonal differences at the perch height. The fieldwork took place monthly from March to December 2011 in the municipality of São Gonçalo do Amarante - Ceará, resulting in a sample of 222 individuals (171 males, 51 females). The perch height for D. gr. microcephalus was similar to that found in other species of the genus. There were no differences between males and females or the stations for the height of the perch; however, adults perched at lower heights than juveniles. Vertical stratification may be linked to abiotic factors such as temperature, relative humidity and/or wind; however, further studies should be conducted in order to test the relationship of these factors with the use of vertical strata. Keywords. vertical stratification, perch height, resource partitioning, Hylid Introduction Most of the studies that approach vertical stratification in anurans make comparative studies between species in a community (Hödl, 1977; Blamires et al., 1997; Pombal, 1997; Rossa-Feres and Jim, 2001; Bertoluci and Rodrigues, 2002; Prado and Pombal, 2005; Melo, Rossa-Feres and Jim, 2007), and they usually address the resource partition space for reproductive purposes, such as calling sites. Consequently, there is a lack of knowledge about intraspecific vertical segregation. Eterovick and Barros (2003) claim that despite the fact that research related to microhabitat use is important for conservation and anuran population monitoring plans such studies are scarce. 1 Programa de Pós-Graduação em Ecologia e Recursos Naturais, Departamento de Biologia, Universidade Federal do Ceará UFC, Av. Humberto Monte, 2977, CEP , Fortaleza, CE, Brazil. 2 Laboratório de Zoologia Experimental, Departamento de Biologia, Universidade Federal do Ceará, Campus do Pici, CEP , Fortaleza, Ceará, Brasil. 3 Núcleo Regional de Ofiologia da Univesidade Federal do Ceará NUROF UFC, Campus do Pici, Bloco 905, CEP: , Fortaleza CE, Brasil. * Corresponding author: patriciamg2003@yahoo.com.br Hylids may constitute the largest proportion of the diversity of anuran species that present vertical stratification in vegetation, since the presence of adhesive discs on their fingertips allows them to explore the vegetation vertically (Cardoso, Andrade and Haddad, 1989; Prado and Pombal Jr., 2005). Despite this adaptation, they may also search other microhabitats, such as rocks and litter, hence being similar to other frogs. Thus, these species of hylids may occupy different microhabitats, allowing for coexistence and minimising competition for resources (Caramaschi, 1981). The hylids present differentiated vertical distribution when correlated with physiological and environmental factors, as well as their body size and mass (Van Sluys and Rocha, 1998 and Prado and Pombal Jr., 2005). Perch height has been studied in hylids such as: Hypsiboas raniceps by Guimarães and Bastos (2003), Hypsiboas albopunctatus by Araújo, Bocchiglieri and Holmes (2007) and Hypsiboas semilineatus by Lisboa et al. (2011). The use of microhabitat, besides varying between different species, may also vary between individuals of the same species, for example, ontogenetically (Alford and Crump, 1982; Eterovick et al., 2010). Freitas et al. (2008) studied the vertical distribution between sexes in the species Phyllomedusa azurea, and it is one of the few studies that has evaluated intraspecific vertical stratification.

2 364 The genus Dendropsophus Fitzinger, 1843 is composed of 95 species and has a wide geographical distribution, occurring from northern Argentina and Uruguay to the south of Mexico, in Central and South America (Amphibiaweb, 2012; Frost, 2012). Dendropsophus gr. microcephalus occurs widely in several phytophysiognomies in the state of Ceará, occurring in coastal tablelands, enclaves of Atlantic Forest and Caatinga (Borges-Nojosa and Cascon, 2005; Lima, 2005; Borges-Nojosa, 2007; Loebmann and Haddad, 2010; Borges-Leite, Borges-Nojosa and Lima, 2012). Several authors have also investigated vertical stratification involving this genus. Muñoz-Guerrero, Serrano and Ramirez-Pinilla (2007) studied the use of microhabitats in four hylids and compared the perch heights of Hypsiboas pugnax, Scarthyla vigilans, Scinax rostratus and Dendropsophus microcephalus. They found a resource space overlap between species of similar sizes. Melo, Rossa-Feres and Jim (2007) also evaluated the perch height for Dendropsophus minutus, D. nanus, D. sanborni and D. elianeae, among other hylids, and they found that calling site heights varied according to the temperature and rainfall. This study investigated the vertical distribution of a population of Dendropsophus gr. microcephalus (Fig. 1) in a forested area of coastal tableland in north-eastern Figure 1. Male of Dendropsophus gr. microcephalus calling. Picture: Luan Pinheiro. Patrícia de Menezes Gondim et al. Brazil. It aimed to answer the following question: does the vertical stratification vary between males and females, juveniles and adults and between the dry and rainy seasons? Materials and Methods We collected specimens at Fazenda Maceió da Taíba (03º S/ 38º W), located in the district of Taíba, municipality of São Gonçalo do Amarante, on the western section Ceará state s coast where Borges- Leite, Borges-Nojosa and Lima (2012) have recorded 23 species of frogs, including nine hylids. We concentrated our collection around a permanent inter-dune pond which shows little level variation, except for periods of great drought when the level may drop by up to 80 percent. The environment in and around the lagoon suffers from strong anthropic action. It has partial native vegetation (semi-deciduous coastal forest) as well as having pioneer vegetation psammophilic I, pioneer vegetation psammophilic II, forest of fixed dunes and rear dunes, vegetation of pre-coastal tablelands and aquatic and marshy vegetation (Figueiredo, 1997). Another part has exotic grasses. The annual averages of temperature and rainfall are 26 C and mm, respectively, and the region s climate is hot tropical, moderate semi-arid (IPECE, 2011). The rainy season runs from January to June with the dry season starting in July and ending in December (Fig. 2) (FUNCEME, 2012). We conducted the fieldwork over a 10 month period from March to December 2011, which consisted of two people in the field for two days each month. Catches were arbitrary, manual and occurred after sunset (6:00pm) until around 11:00pm. For each individual collected, we recorded the occurrence of calling activity and the perch height on vegetation using a measuring tape (1 cm accuracy). For individuals perched above the water, we considered the perch height to be the distance above the water s surface. We euthanized the anurans in the field with dermatologic anaesthetic ointment of lidocaine 50 mg/g and weighed them with a precision balance (0.01 g accuracy). We measured the snout-vent length (SVL) with the aid of digital callipers (0.01 mm accuracy). The collected individuals were then fixed with 10% formalin. After dissection in the laboratory, we sexed the animals through direct observation of the gonads. The specimens were deposited in the Herpetology Collection of the Universidade Federal do Ceará (CHUFC) (Appendix). We considered the male with the shortest SVL (SVL mm) to be a criterion to identify individuals and

3 Microhabitat use (vertical distribution) by a population of Dendropsophus 365 Figure 2. Average monthly temperature and monthly precipitation in 2011 for the study site. Source: Fundação Cearense de Meteorologia e Recursos Hídricos (FUNCEME). young adults, and for the females, we considered the smallest individual with mature eggs (SVL mm) to be a defining criterion for adulthood. In order to investigate the relationship between perch height, sex, ontogeny and season, we used a nonparametric technique of regression known as GLM (Generalised Linear Model) with the use of the Gamma distribution. We included SVL and body mass as covariates. The model went through a stepwise technique, which removed all non-significant parameters. In order to evaluate whether the model was a good fit, through its dispersion, we performed an analysis of deviation (ANODEV), which uses shift values for each explanatory variable and the corresponding chi-square tests. The significance of the model is given as it adds each variable tested. We chose the value of 0.05 as the limit of significance. We have presented the values such as mean ± standard deviation followed by the minimum and maximum value and the number of specimens measured. We performed all the statistical analyses using the statistics program R (R Development Core Team, 2008). Results We collected a total of 222 individuals of Dendropsophus gr. microcephalus during the sampling period, of which there were 171 males (158 adults and 13 juveniles) and 51 females (16 adults and 35 juveniles). The average perch height on vegetation for the population was ± cm (0-185; n = 222). For females, the average perch height was ± cm (1-185; n = 16) and for males, it was ± cm (0-160; n = 158).The juveniles average perch height was ± cm (1-185; n = 48), and for adults, it was ± cm (0-135; n = 174). The average perch height in the dry season was ± cm (0-185; n = 124), and during the rainy season it was ± cm (0,5-93; n = 98). According to the result of GLM, there was an ontogenetic difference for the perch height (T=3.78; p<0.001). However, there was no seasonal or sexual difference for the perch height. Furthermore, the SVL and body mass did not influence the vertical distribution. Discussion The average perch height in the herbaceous layer for Dendropsophus gr. microcephalus recorded in this study (29.13 cm) was similar to that found for other species of the genus. Muñoz-Guerrero, Serrano and Ramírez- Pinilla (2007) found a perch height between 40 and 50 cm for Dendropsophus microcephalus. Menin, Rossa- Feres and Giaretta (2005) found heights between 20.1 cm and 50.6 cm for D. nanus and 43.3 cm and 54.2 cm for D. sanborni. The average perch found by Afonso and Eterovick (2007) for D. minutus was 15 cm, whereas Eterovick et al. (2010) found it to be 50 cm whilst for D. seniculus it was 33 cm. In the studies cited above, there was variation in the average perch height between 15 cm and 50.6 cm for the genus Dendropsophus, a similar

4 366 Patrícia de Menezes Gondim et al. Figure 3. Sexual, ontogenetic and seasonal comparison of perch height for Dendropsophus gr. microcephalus in a coastal tableland area, São Gonçalo do Amarante, Ceará, from March to December Box plots showing median, quartiles and extremes and averages in red. range to the average found for D. gr. microcephalus in this study. Eterovick et al. (2010) showed that, in adulthood, some related species may make similar use of microhabitats, which included the height above ground as one of the criteria for the definition. In contrast, populations of the same species may differ in microhabitat use from place to place, as for D. minutus. Therefore, we can conclude that microhabitat use in anurans is a plastic and variable trait, and is of little use for phylogenetic inferences (Eterovick et al., 2010). Muñoz-Guerrero, Serrano and Ramírez-Pinilla (2007) claim that perch height is a factor related to segregation between species of similar body size in order to avoid niche overlap. Likewise, it is possible that comparisons between categories within the same species may also reveal vertical stratification, such as the ontogenetic variation found in D. gr. microcephalus in this work. Intersexual differences in relation to the vertical position (perch height) have been investigated in Phyllomedusa azurea, but no differences were found between the perch heights taken by each sex (Freitas et al., 2008). In this study, we did not find differences between males and females for their perch heights; however, Dendropsophus gr. microcephalus adults perched at lower average heights than the juveniles. The ontogenetic variation has contributed to a reduction in the overlap in the use of vertical strata. Although SVL and body mass were not significant in explaining the occupation of greater heights for juveniles compared to adults, it is possible that a discrepancy in the samples between the groups may have caused a bias that has limited the obtaining of a significant relationship of these parameters to perch height. Muñoz-Guerrero, Serrano and Ramírez-Pinilla (2007) observed that the overlap in habitat use between four sympatric species of hylid was minimised by the differentiated use of microhabitat related to body size. In Oliveira (2011), D. werneri exhibited higher amplitude in the use of vertical strata of vegetation than D. elegans, D. microps, and D. minutus, which are species of smaller size and mass. Abiotic factors may also explain variations in perch height of the species. Prado and Pombal Jr. (2005), when studying spatial and temporal distribution of anurans in a swamp in the Reserva Biológica de Duas Bocas, SE, Brazil, related factors such as relative humidity, temperature and wind to the vertical distribution of the hylid species for that community and indicated that physiological differences, such as temperature tolerance and water loss, may reflect in the selection of the microenvironment. Melo, Rossa-Feres and Jim (2007) claim that the vertical distribution of hylids varied mainly due to temperature, possibly because it is slightly higher near the ground or water body. The abiotic factors mentioned here possibly explain how individuals of D. gr. microcephalus are distributed vertically. This paper shows that the population of D. gr. microcephalus located in forest vegetation of a coastal tableland perches in the herbaceous layer at an average height similar to that found in studies for other species of the same genus. Ontogenetic variation may be related to a reduction in the overlap in the use of vertical strata for adults and juveniles. There were no seasonal and

5 Microhabitat use (vertical distribution) by a population of Dendropsophus 367 sexual differences for the perch height. The use of vertical strata may be linked to abiotic factors such as temperature, relative humidity and wind, among others. More studies are needed to confirm the influence of these factors on vertical distribution. Acknowledgements. We would like to thank Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for granting collecting permits (authorization # SISBIO); Mr. and Mrs. Borges for their hospitality during field work; D. O. Soares, D. O. Moraes and C. H. Bezerra for help in the field; and J. F. M. Rodrigues and D. Zanchi for manuscript review and suggestions. P. M. Gondim thanks her sister, P. M. Gondim, for help in translating the manuscript into English and the Graduate Program in Ecology and Natural Resources for the Master s degree. References Afonso, L.G., Eterovick, P.C. (2007): Microhabitat choice and differential use by anurans in forest streams in southeastern Brazil. Journal of Natural History 41: Alford, R.A., Crump, M.L. 1982: Habitat partitioning among size classes of larval southern leopard frogs, Rana utricularia. Copeia 1982 (2): Amphibiaweb (2012): Information on Amphibian Biology and Conservation. Available at: Last accessed on 21 June Araújo, F.R.R.C., Bocchiglieri, A., Holmes, R.M. (2007): Aspectos ecológicos de Hypsiboas albopunctatus (Anura, Hylidae) no Brasil central. Neotropical Biology and Conservation 2(3): Bertoluci, J., Rodrigues, M.T. (2002): Utilização de hábitats reprodutivos e micro-hábitats de vocalização em uma taxocenose de anuros (Amphibia) da Mata Atlântica do sudeste do Brasil. Papéis Avulsos de Zoologia 42(11): Blamires, D., Motta, J.A.O., Souza, K.G., Bastos, R.P. (1997): Padrões de distribuição e análise de canto em uma comunidade de anuros no Brasil Central. In: Contribuição ao conhecimento ecológico do Cerrado Trabalhos selecionados do 3º Congresso de Ecologia do Brasil, p Leite, L.L, Saito, C.H., Eds., Departamento de Ecologia Universidade de Brasília, Brasília, Brasil. Borges-Leite, M.J., Borges-Nojosa, D.M., Lima, D.C. (2012): Guia de Anfíbios e Répteis em São Gonçalo do Amarante, 1º Edição. Fortaleza, Dedo de Moças Editora e Comunicação Ltda. 128 pp. Borges-Nojosa, D.M. (2007): Diversidade de anfíbios e répteis da Serra de Baturité, Ceará. In: Diversidade e conservação da biota na Serra de Baturité, Ceará, p OLIVEIRA, T.S., ARAÚJO, F.S., Eds., 1 a.ed., Fortaleza, Edições UFC. Borges-Nojosa, D.M., Cascon, P. (2005): Herpetofauna da área reserva da Serra das Almas, Ceará. In: Análise das variações da biodiversidade do bioma Caatinga, p Araújo, F.S., Rodal, M.J.N., Barbosa, M.R.V., Eds., 1º.ed., Brasília, Ministério do Meio Ambiente. Caramaschi, U. (1981): Variação estacional, distribuição espacial e alimentação de populações de hilídeos na represa do rio Pardo (Botucatu, SP) (Amphibia, Anura, Hylidae). Unpublished dissertation, Universidade Estadual de Campinas, Campinas,139 pp. Cardoso, A.J., Andrade, G.V., Haddad, C.F.B. (1989): Distribuição espacial em comunidades de anfíbios (Anura) no sudeste do Brasil. Revista Brasileira de Biologia 49(1): Eterovick, P.C., Barros, I.S. (2003): Niche occupancy in southeastern Brazilian tadpole communities in montane-meadow streams. Journal of Tropical Ecology 19: Eterovick, P.C., Rievers, C.R., Kopp, K., Wachlevski, M., Franco, B.P., Dias, C.J., Barata, I.M., Ferreira, A.D.M., Afonso, L.G. (2010): Lack of phylogenetic signal in the variation in anuran microhabitat use in southeastern Brazil. Evolutionary Ecology 24: Figueiredo, M.A. (1997): Unidades Fitoecológicas. In: Atlas do Ceará, p Iplance, Ed., Fundação Instituto de Planejamento do Ceará/Governo do Estado do Ceará, Fortaleza, Brasil. Freitas, E.B., De-Carvalho, C.B., Faria, R.G., Batista, R.C., Batista, C.C., Coelho, W.A., Bocchiglieri, A. (2008): Nicho ecológico e aspectos da história natural de Phyllomedusa azurea (Anura: Hylidae, Phyllomedusinae) no Cerrado do Brasil Central. Biota Neotropica 8(4): Frost, D.R. (2012): Amphibian Species of the World: an Online Reference. Version 5.5, (31 January, 2011). Available at: American Museum of Natural History, New York, USA. Last accessed on 11 March Fundação Cearense de Meteorologia e Recursos Hídricos (FUNCEME) (2012): Available at: Last accessed on 29 May Guimarães, L. Dall A., Bastos, R.P. (2003): Vocalizações e interações acústicas em Hyla raniceps (Anura, Hylidae) durante a atividade reprodutiva. Iheringia, Série Zoologia 93(2): Hödl, W. (1977): Call differences and calling site segregation in anuran species from Central Amazonian floating meadows. Oecologia 28(4): Instituto de Pesquisa e Estratégia Econômica do Ceará (IPECE) (2011): Perfil Básico Municipal - São Gonçalo do Amarante. Fortaleza, 18 pp. Lima, D.C. (2005): A bananicultura na Área de Proteção Ambiental da Serra de Maranguape-CE e suas implicações no ambiente físico, humano e na biodiversidade. Unpublished dissertation, Universidade Federal do Ceará, Ceará, 107 pp. Lisboa, E.B.F. Moura, G.J.B., Melo, I.V.C., Andrade, E.V.E., Figuerêdo Júnior, J.M. (2011): Ecologia de Hypsiboas semilineatus (SPIX, 1824) (Amphibia, Anura, Hylidae) em remanescente de Mata Atlântica, Nordeste do Brasil. Revista Ibero-Americana de Ciências Ambientais 2(1): Loebmann, D., Haddad, C.F.B. (2010): Amphibians and reptiles from a highly diverse area of the Caatinga domain: composition and conservation implications. Biota Neotropica 10: Melo, G.V., Rossa-Feres, D.C., JIM, J. (2007): Variação temporal no sítio de vocalização em uma comunidade de anuros de Botucatu, Estado de São Paulo, Brasil. Biota Neotropica 7(2):

6 368 Patrícia de Menezes Gondim et al. Menin, M., Rossa-Feres, D.C., Giaretta, A.A. (2005): Resource use and coexistence of two syntopic frogs (Anura, Hylidae). Revista Brasileira de Zoologia 22(1): Muñoz-Guerrero, J., Serrano, V.H., Ramírez-Pinilla, M.P. (2007): Uso de microhábitat, dieta, y tiempo de actividad en cuatro espécies simpátricas de ranas hílidas neotropicales (Anura: Hylidae). Caldasia 29(2): Oliveira, I.S. (2011): Sítio de vocalização, dominância e girino de Dendropsophus werneri (Cochran, 1952) e análise citogenética de quatro espécies sintópicas de Dendropsophus em área de floresta Atlântica no Paraná. Unpublished dissertation, Universidade Federal do Paraná, Curitiba, 91 pp. Pombal Jr., J.P. (1997): Distribuição espacial e temporal de anuros (Amphibia) em uma poça permanente na Serra de Paranapiacaba, sudeste do Brasil. Revista Brasileira de Biologia 57(4): Prado, G.M., Pombal Jr., J.P. (2005): Distribuição espacial e temporal dos anuros em um brejo da reserva biológica de Duas Bocas, sudeste do Brasil. Arquivos do Museu Nacional 63(4): R Development Core Team (2008): R: A language and environment for statistical computing. Austria: R Foundation for Statistical Computing. Available at: org. Rossa-Feres, D.C., Jim, J. (2001): Similaridade do sítio de vocalização em uma comunidade de anfíbios anuros na região noroeste do Estado de São Paulo, Brasil. Revista Brasileira de Zoologia 18(2): Van Sluys, M., Rocha, C.F.D. (1998): Feeding habits and microhabitat utilization by two syntopic Brazilian Amazonian frogs (Hyla minuta and Pseudopaludicula sp. (gr. falcipes). Revista Brasileira de Biologia 58(4): Appendix Listed individuals collected during this study and deposited in the Herpetology Collection of the Universidade Federal do Ceará (CHUFC). Dendropsophus gr. microcephalus: CHUFC A ; CHUFC A 5911; CHUFC A 6009; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A 6187; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A ; CHUFC A Accepted by Philip de Pous