Ontogeny and Behavioural Aspects of the Tadpoles of Megaelosia Goeldii (Baumann, 1912) (Amphibia, Anura, Hylodidae)

Herpetology Notes, volume 11: 629-639 (2018) (published online on 20 August 2018) Ontogeny and behavioural aspects of the tadpoles of Megaelosia goeldii (Baumann, 1912) (Amphibia, Anura, Hylodidae) Dener das Neves da Silva1, Felipe Cesar Barros da Rosa¹ and Ana Maria Paulino Telles de Carvalho-e-Silva¹,* Abstract. The genus Megaelosia consists of large size, diurnal stream-breeder species. Although the tadpole of M. goeldii had been described, its ontogeny and behaviour were never detailed. Here, we describe the development of the M. goeldii larvae, as well as some behavioural aspects. Tadpoles were collected between 1983 and 2015 in the municipality of Teresópolis, state of Rio de Janeiro, Brazil. Stages were determined based on Gosner’s table. Tadpoles present accentuated growth on stage 25, but a slow growth from stages 26 to 42. Changes in coloration were observed throughout the tadpole development. Larvae were found in streams of running water, in approximately 1.0–1.2 m depth. During the day they hide among stones in the bottom, and at night they are easily spotted in shallower waters, foraging near the surface. Larvae are observed throughout the year, although the smaller ones are mostly found in August and September, indicating that reproduction occurs in the winter. The tadpoles showed emetic behaviour when collected, probably due to the exposure to stress situations or to scare away predators. We analysed 208 specimens (stages 25 to 40), and 71% presented depigmentation in the oral disc; this phenomenon was more frequently observed in larger tadpoles. The oral depigmentation in these tadpoles indicates the presence of the fungus Batrachochytrium dendrobatidis (Bd), one of the main responsible for the worldwide decline of amphibians. The presence of Bd zoosporangia in the oral disc of M. goeldii tadpoles were detected with histological investigation. Keywords. development, emetic behaviour, natural history, chytridiomycosis Introduction Alamillo, 2005; Costa et al., 2010; Alcalde et al., 2011; Fabrezi, 2011; Vera Candioti et al., 2011; Mongin and The morphology and biology of tadpoles attract Carvalho-e-SiIva, 2013). the interest of researchers from different areas. For The family Hylodidae Gunther 1858 is currently example, including information about larval traits and composed of the genera Crossodactylus Duméril and habits on systematics studies, not only helps in the Bibron 1841, Hylodes Fitzinger 1826 and Megaelosia identification of several amphibian species but also can Miranda-Ribeiro 1923, forming a well-defined be used to improve our understanding on phylogenetic monophyletic group (Frost et al., 2006; Grant et al., relationships (Hall et al., 1997). In addition, detailed 2006; Pyron and Wiens, 2011), totalizing 46 species descriptions of ontogeny are important tools for (Frost, 2017). Both adult and larval forms are restricted comparing the growth patterns of different amphibian to streams of the Atlantic Rainforest (Pombal et al., taxa (Costa et al., 2010). Recent studies have focused on 2003; Haddad and Prado, 2005; Lingnau et al., 2008; the importance of tadpoles using different approaches, Silva and Benmaman, 2008). i.e. anatomy, morphology, ecology and even phylogenies The genus Megaelosia comprises large-sized and solely based in larval characters (Haas, 2003; Sheil and diurnal species, associated with lotic sites (Giaretta et al., 1993). All seven species in the genus are restricted to a limited area of the Atlantic Rainforest, in the southeastern Brazil: Megaelosia apuana Pombal, Prado and Canedo 2003; Megaelosia bocainensis Giaretta, ¹ Laboratório de Biossistemática de Anfíbios, Departamento Bokermann and Haddad 1993; Megaelosia boticariana de Zoologia, Instituto de Biologia, Centro de Ciências Biológicas e da Saúde, Universidade Federal do Estado do Giaretta and Aguiar 1998; Megaelosia goeldii Rio de Janeiro, 22290-240, Rio de Janeiro, RJ, Brasil. (Baumann 1912); Megaelosia jordanensis (Heyer * Corresponding author. Email: [email protected] 1983); Megaelosia lutzae Izecksohn and Gouvêa 1987 630 Dener das Neves da Silva et al. and Megaelosia massarti (De Witte 1930). Specimens isolated from tadpoles with depigmented mouthparts of Megaelosia are extremely rare in scientific collections across Brazil’s Atlantic forest (Jenkinson et al., 2016). due to their restricted geographical ranges, cryptic Therefore, patterns of mouthparts depigmentation can behaviour (Giaretta et al., 1993; Melo et al., 1995) and be effectively used as a proxy for Bd infections in Brazil low-density populations (Pombal et al., 2003). They are (Carvalho et al., 2017). very agile animals, exhibiting a rapid response of diving There are no studies regarding the ontogeny of any of in lotic waters when perturbed, consequently reducing the species in the genus Megaelosia. The tadpole of M. the chance of being captured (Miranda-Ribeiro, 1923; goeldii was described by Lutz (1930) and redescribed by Izecksohn and Gouvêa, 1985). Nuin (2003), but its ontogeny and behaviour were never The emesis capacity is a behavioural aspect described detailed. In the present study, we describe the larval for vertebrates and are present in mammals (Borison development of M. goeldii, considering its behavioural and Wang, 1953; Andrews et al., 1990), reptiles (Gans, aspects. We also discuss the evidence of the fungus 1952), birds (Matthews, 1949; Saxena et al., 1977), fish Bd on M. goeldii larvae and the possible consequence (Tiersch and Griffith, 1988; Andrews et al., 1998) and for tadpole growth. We expect larger tadpoles to have amphibians (Naitoh et al., 1989; Naitoh and Wassersug, higher Bd prevalence because they have been inhabiting 1994). In general, vomiting is a defensive mechanism the aquatic habitat for longer and therefore might to eliminate toxins when accidentally ingested (Lang et have been more exposed to Bd zoospores than smaller al., 1986). However, Gans (1952) describes a selective tadpoles. emesis of eggshell performed by snakes from Dasypeltis Wagler 1830 genus frequently carried out to avoid Materials and Methods predation. Naitoh et al. (1989) shows that in anurans, the ability to vomit only occurs after metamorphosis, We examined 215 tadpoles of M. goeldii, collected because tadpoles do not have the necessary features to in sporadic events between 1983 and 2015 at the increase their abdominal pressure and vomit. Parque Nacional da Serra dos Órgãos (PARNASO) Chytridiomycosis is an emergent disease caused - “National Park of Serra dos Órgãos” (22°26’54’’S, by the Chytridiomycota fungus, Batrachochytrium 42°59’01’’W) and the adjacent locality of Vale da dendrobatidis (Bd) Longcore, Pessier and Nichols Revolta (22°26’00’’S, 42°56’00’’W), both belonging 1999. Declines and mass extinctions associated with Bd to the municipality of Teresópolis, Rio de Janeiro state, was reported in Australia (Berger et al., 1998), South Brazil. America (Carvalho et al., 2017), Central America We captured tadpoles using sieves and funnel traps. (Lips 1999), North America (Muths et al., 2003) and After capture, individuals were anesthetized with Europe (Bosch et al., 2001). This pathogenic fungus chloretone 5% (from 1983 until 2011 by A.M.P.T. (Bd) has flagellated aquatic zoospores with a potential Carvalho-e-Silva) and lidocaine 2%, (from 2012 until to rapidly spread within water (Longcore et al., 1999), 2015 by A.M.P.T. Carvalho-e-Silva, F.B. Rosa and facilitating tadpoles infection. B. dendrobatidis infects D.N. Silva), fixed and preserved in 5% formalin. The the keratinizing tissue of amphibians, which in tadpoles identification of tadpoles was based on specimens reared is concentrated in the mouthparts (Berger et al., 1998). in aquarium until metamorphosis and on literature (Lutz The depigmentation pattern in tadpoles due to Bd 1930; Nuin 2003). Observation on the behaviour of infection is unequivocal, although depigmentation tadpoles reared in the laboratory also improved and may also be a result of the exposure to environmental corroborated our in situ observations. The depth of the contaminants (Hayes et al., 1997; Rowe et al., 1998) sampling sites was taken with a standard measuring or due to low temperatures (Rachowicz, 2002). B. tape. The analysed material (see Appendix) is stored in dendrobatidis causes patchy depigmentation with the amphibian collections of Universidade Federal do complete loss of keratin in localized areas compared Estado do Rio de Janeiro (UNIRIO) and Universidade with fully keratinized surrounding areas (Fellers et Federal do Rio de Janeiro (UFRJ/ZUFRJ). al., 2001). Recent studies found a huge proportion of Some specimens were fixed with the mouth open in tadpoles with highly depigmented mouthparts attributed order to evaluate the oral morphology, applying the to Bd. The prevalence of infection was estimated at 95% technique of Carvalho-e-Silva and Carvalho-e-Silva in the Atlantic forest torrent frog Hylodes cf. ornatus (1994). Tadpoles were measured with digital caliper and Lithobates catesbeianus (Shaw 1802) (Vieira et ruler (precision 0.1 mm). The measurements and al., 2013). Thus, more than 100 Bd genotypes were nomenclature were adapted from Altig and McDiarmid Ontogeny and behavioural aspects of the tadpoles of Megaelosia goeldii 631 Figure 1. Mean values of total length (TL), body length (BL) Figure 2. Mean values of body height (BH) and tail height and tail length (TAL) of Megaelosia goeldii tadpoles in the (TH) of Megaelosia goeldii tadpoles in the Gosner stages 25 Gosner stages 25 to 46. to 46. (1999):

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