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Occurrence and Egg-Laying of Leptodactylus Macrosternum Miranda-Ribeiro, 1926 in Mangrove Habitat in Ceará, Northeast Brazil

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Occurrence and Egg-Laying of Leptodactylus Macrosternum Miranda-Ribeiro, 1926 in Mangrove Habitat in Ceará, Northeast Brazil Herpetology Notes, volume 12: 865-868 (2019) (published online on 12 August 2019) Occurrence and egg-laying of Leptodactylus macrosternum Miranda-Ribeiro, 1926 in mangrove habitat in Ceará, Northeast Brazil Alexander Cesar Ferreira1, Paulo Cascon2,*, and Helena Matthews-Cascon2 Most amphibians are poor osmoregulators and taxa—L. fuscus (Schneider, 1799); L. latrans (Steffen, particularly sensitive to water salinity, conditions 1815); L. macrosternum Miranda-Ribeiro, 1926; L. which generally exclude them from brackish and saline pentadactylus (Laurenti, 1768); and L. vastus Lutz, environments (Gomez-Mestre et al., 2004). However, 1930—have been reported living in association with some species are able to tolerate elevated salinity mangroves (Crawford and Jones 1933; Loebmann and and persist in brackish (salinity between 0.5 and 32 Mai 2008; Ferreira and Tonini, 2010; Brito et al. 2011; ppt) conditions, and to date ~144 species have been Silva and Fernandes 2016). reported from such environments (Balinsky, 1981; Wu Leptodactylus macrosternum belongs to the L. latrans and Kam, 2009; Hopkins and Brodie Jr, 2015; Chang group (de Sá et al., 2014) and is reported from Colombia, et al., 2016). Larvae of the palmate newt Lissotriton Venezuela and the Guianas, south through Brazil and helveticus (Razoumowsky, 1789) have been found in Bolivia (Gallardo, 1964; Frost, 1985; De la Riva and saline waters close to 22 ppt (Spurway, 1943; Hopkins Maldonado, 1999). Here, we report the presence and and Brodie Jr, 2015) while one anuran, the crab-eating breeding activity of L. macrosternum in mangrove frog Fejervarya cancrivora (Gravenhorst, 1829) has habitat in a coastal region of Ceará, Northeast Brazil. extreme saline-tolerance, living in salinities up to 35 ppt Our observations were made at 08:35 h on 7th May (Hopkins and Brodie Jr, 2015). At least 22 species of 2018, in a sea level swamp within an abandoned anurans (including F. cancrivora) have been reported saltwork in the margins of Pacoti River, Municipality of as living in or in close proximity to mangrove habitat, Eusebio, in the metropolitan region of Fortaleza, state around half of them in the Neotropics (Hopkins and of Ceará, Northeast Brazil (3.8299° S, 38.4217° W; Brodie Jr, 2015). WGS84) (Fig. 1). The climate of the region is tropical The Neotropical genus Leptodactylus Fitzinger, with a wet season from February to June and an average 1826 includes 74 widely distributed taxa, ranging annual rainfall below 875 mm (Barreto et al., 2012). from southern North America, throughout most of At the site we observed an adult L. macrosternum South America to central Argentina (Frost, 2018). apparently guarding an egg mass (likely female, since Leptodactylids occur in a range of riparian to terrestrial in this genus females exhibit parental care of eggs; habitats (Heyer, 1969; de Sá et al., 2014), five of which Martins 2001; Prado et al., 2000; Prado et al., 2002; Prado and Haddad, 2003; Santos and Amorim, 2006; Filho and Giaretta, 2008; Castro et al., 2013) spread among herbaceous saltwort Batis maritima L. within a patch of mangrove Avicennia germinans L. (Fig. 2). Vocalisations from several conspecifics were heard in 1 Instituto de Ciências do Mar (LABOMAR), Universidade the immediate vicinity, where further egg masses were Federal do Ceará – Av. da Abolição 3207, 60165-081, also seen. No other anurans were observed. Fortaleza, Ceará, Brazil / Tropical Marine Sciences The observation locality (Fig. 1–2) has periodic Postgraduate Program (PPGCMT, PNPD / CAPES). 2 Departamento de Biologia, Universidade Federal do Ceará intrusion of tidal water from the Pacoti River estuary, – Campus do Pici, 60440-900, Fortaleza, Ceará, Brazil. mainly from spring tides. Measures of the interstitial * Corresponding author. E-mail: [email protected] soil salinity (made with an optical refractometer at the 866 Alexander Cesar Ferreira et al. Figure 1. Geographic location of the study site in Brazil where Leptodactylus macrosternum reproductive activity was observed. (A) coastal locality of site in Ceará State, Northeast Brazil; (B) satellite image of the site, inset with the area comprising the now defunct saltwork, northwest of the Pacoti River. The saltwork is surrounded by mangroves within which the specific locality of the observation is circled. Panel B images generated via Google Earth. same site where egg masses were observed) show that habitat (Crawford and Jones, 1933; Loebmann and Mai, salinity can drop to 5 ppt in the rainy season, and reach 2008; Silva and Fernandes, 2016), our observation is, to more than 60 ppt in the dry season. To our knowledge our knowledge, the first to report reproductive activity L. macrosternum has only been observed at this location in this environment. To clarify taxonomic affinity and during the rainy season and it is assumed that conditions verify breeding success, in coming seasons we aim to (e.g., salinity of ~60 ppt) outside this period restrict the collect voucher specimens of larvae and monitor the site presence of amphibians. The breeding pattern of L. for successful larval metamorphosis. macrosternum is strongly driven by seasonal cycles; frogs may aestivate during dry periods, emerging to References breed at the onset of rains (Dixon and Staton, 1976). Balinsky, J.B. (1981): Adaptation of nitrogen metabolism to Intriguingly, in a previous rainy season we observed hypertonic environment in Amphibia. Journal of Experimental tadpoles of unconfirmed taxonomic affinity in the Zoology 215: 335–350. brackish waters between mangrove trees at the same Barreto, H.B.F., Santos, W.O., Cruz, C.M. (2012): Análise da site. distribuição da precipitação pluviométrica média anual no estado Leptodactylid taxa reported to breed in saline habitats do Ceará. Revista Verde de Agroecologia e Desenvolvimento Sustentável 7: 122–128. include L. albilabris (brackish swamp/forest in Puerto Brito, A.L.R., Silva, R.P., Fernandes, M.E.B. (2011): Leptodactylus Rico) and L. melanonotus (beach ponds in Costa fuscus (whistling frog). Habitat and diet. Herpetological Review Rica) (Hopkins and Brodie Jr, 2015). Although L. 42: 88. macrosternum has been previously recorded in mangrove Castro, D.P., Borges-Leite, M.J., Lima, D.C., Borges-Nojosa, D.M. Occurrence and egg-laying of Leptodactylus macrosternumt in Brazil 867 Figure 2. Observations of Leptodactylus macrosternum reproductive activity within mangrove habitat of the saltwork. (A) The Avicennia germinans mangrove habitat (centre) where we made our observations; (B) the captured adult frog found guarding spawn; (C) egg mass at the base of an A. germinans mangrove, and spread among mangrove pneumatophores; (D) further view of an egg mass between herbaceous Batis maritima. Photographs by A. C. Ferreira. (2013): Parental care in two species of Leptodactylus Fitzinger, Dixon, R.J., Staton, M.A. (1976): Some aspects of the biology 1826 (Anura, Leptodactylidae) in north-eastern Brazil. of Leptodactylus macrosternum Miranda-Ribeiro (Anura: Herpetology Notes 6: 267–269. Leptodactylidae) on the Venezuelan llanos. Herpetologica 32: Chang, Y., Wu, C., Huang, Y., Sung, S., Hwang, W. (2016): 227–232. Occurrence and reproduction of anurans in brackish water in Ferreira, R.B., Tonini, J.F.R. (2010): Living holed: Leptodactylus a coastal windbreak forest in Taiwan. Herpetology Notes 9: latrans occupying crabs’ burrows. Herpetology Notes 3: 237– 291–295. 238. Crawford, S.C., Jones, E.P. (1933): Field notes on some amphibians Filho, J.G.O., Giaretta, A.A. (2008): Reproductive behavior of from British Guiana. Copeia 2: 88–92. Leptodactylus mystacinus (Anura, Leptodactylidae) with notes De la Riva, I., Maldonado, M. (1999): First record of Leptodactylus on courtship call of other Leptodactylus species. Iheringia 98: ocellatus (Linnaeus, 1758) (Amphibia, Anura, Leptodactylidae) 508–515. in Bolivia and comments on related species. Graellsia 55: 193– Frost, D.R. (1985): Amphibian species of the world. A taxonomic 197. and geographical reference. Lawrence, Allen Press and the de Sá, R.O., Grant, T., Camargo, A., Heyer, W.R., ASC. Ponssa, M.L., Stanley, E.L. (2014): Systematics of the Frost, D.R. (2018): Amphibian Species of the World: an Online Neotropical genus Leptodactylus Fitzinger, 1826 (Anura: Reference. Version 6.0. Electronic Database. Available at: http:// Leptodactylidae): Phylogeny, the relevance of non-molecular research.amnh.org/herpetology/amphibia/index.html. American evidence, and species accounts. South American Journal of Museum of Natural History, New York, USA. Accessed on 31 Herpetology 9 (Spec. Issue 1): 1– 128. July 2018. 868 Alexander Cesar Ferreira et al. Gallardo, J.M. (1964): Consideraciones sobre Leptodactylus Prado, C.P.A., Uetanabaro, M., Haddad, C.F.B. (2002): ocellatus (L.) (Amphibia, Anura) y especies aliadas. Physis 24: Description of a New Reproductive Mode in Leptodactylus 373–384. (Anura, Leptodactylidae), with a Review of the Reproductive Gomez-Mestre, L., Tejedo, M., Ramayo, E., Estepa, J. (2004): Specialization toward Terrestriality in the Genus. Copeia 4: Developmental alterations and osmoregulatory physiology 1128–1133. of a larval anuran under osmotic stress. Physiological and Santos, E.M., Amorim, F.O. (2006): Cuidado parental em Biochemical Zoology 77: 267–274. Leptodactylus natalensis (Amphibia, Anura, Leptodactylidae). Heyer, W.R. (1969): The adaptive ecology of the species groups Iheringia 96: 491–494. of the genus Leptodactylus (Amphibia, Leptodactylidae). Silva, R.P., Fernandes, M.E.B. (2016): Anfíbios e répteis.
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