Elachistocleis helianneae Caramaschi, 2010

Dias-Souza, Marcos Roberto, Costa-Campos, Carlos Eduardo & Menin, Marcelo, 2019, The tadpole of Elachistocleis helianneae Caramaschi, 2010 (Anura: Microhylidae), Zootaxa 4701 (6), pp. 594-600 : 594-599

Elachistocleis helianneae Caramaschi

is a recently described species from Humaitá, state of Amazonas, Brazil. This species is also found in the Brazilian states of Pará, Amapá, and Rondônia, and in northeastern Bolivia ( Caramaschi 2010; Costa-Campos & Freire 2015; Frost 2019). Adults of this species reproduce during the rainy season in temporary ponds located in open areas or near the forest border ( Lima et al. 2012). Here we present a detailed description of the tadpole of E. helianneae collected from two localities in the Brazilian Amazonia (the city of Manaus and Macapá).

Adults and 56 tadpoles of E. helianneae were collected in April and May of 2019 at the Campus of the Universidade Federal do Amapá (Campus UNIFAP: 00°00′24.30″S, 51°05′9.13″W), municipality of Macapá, State of Amapá. These specimens are deposited in the Herpetological Collection of the Universidade Federal do Amapá (tadpoles lot CECC 3461/3465, adults CECC 2768-male; 2778-female) and in the Coleção Zoológica Paulo Bührnheim of the Universidade Federal do Amazonas, section larvae of anurans - CZPB-LA (tadpole lot 419/886). The other three tadpoles were collected in January and February of 2005 at the Reserva Florestal Adolpho Ducke ( RFAD: between 02º55′ and 03º01′S, between 59º53′ and 59º59′W), municipality of Manaus, State of Amazonas ( CZPB-LA tadpole lots 417/884 and 418/885). At both collection sites, tadpoles were found in temporary ponds at the border of unflooded terra firme forests. An amplectant pair was brought to the laboratory to spawn, allowing us to confirm the identity of the tadpoles previously collected in the field. The tadpoles were maintained in a glass container filled with water collected from a temporary pond. All individuals were anesthetized in 5% lidocaine and preserved in 1:1 solution of ethanol 70% and formalin 15 %.

The developmental stages were determined according to Gosner (1960). The terminology, measurements and diagnostic characters followed Altig & McDiarmid (1999) while the ontogenetic variation in spiracle and vent tube followed Lavilla & Langone (1991). Measurements were obtained using a stereoscopic microscope equipped with a micrometric ocular (measures to the nearest 0.01 mm); the tadpoles in advanced development stage were measured using a Mitutoyo digital caliper (0.01 mm precision). The morphometric measurements are: total length (TL), body length ( BL), tail length ( TAL), body width ( BW), body height (BH), width of head ( HWLE), tail muscle width ( TMW), maximum tail height ( MTH), tail muscle height ( TMH), interorbital distance ( IOD), internarial distance ( IND), eye-nostril distance ( END), nostril-snout distance ( NSD), eye diameter ( ED), vent-tube length ( VTL), spiracle-tube length ( STL), and oral disc width ( ODW). IND, END, and NSD were measured from the external nostrils visible as rounded whitish spot and located dorsally in tadpoles at Gosner Stages 36–39 and from the perforated nostrils in tadpoles at Stage 40.

Description. The description is based on five tadpoles at stage 36 (CZPB-LA 419/886; CECC 3461/3465). Measurements of all specimens are listed in Table 1. Body triangular/depressed in lateral view ( Fig. 1A ), elongate oval in dorsal and ventral views ( Fig. 1B and C ), and wider than deep. Body and tail measuring 37.5% and 62.5% of the total length, respectively. Body highest at its posterior third and wider immediately posterior to eyes. Snout rounded in dorsal, ventral, and lateral views. Eyes small, representing 28.1% of the body height, located and directed laterally, visible dorsally and ventrally. Nostrils absent. Mouth terminal, tooth rows, jaw sheaths, and papillae absent. Upper lip fleshy, formed by two dermal flaps notched medially, edges not jagged, and covering the lower lip ( Fig. 1D ). Lower lip narrow, fleshy, and Ushaped ( Fig. 1E ). Spiracle ventral, single, positioned medially and ventrally ( Fig. 1F ). Spiracle opening large, directed to the left side of the ventral fin, and with distal border projecting over the vent tube. Vent tube long, medial, and fused to the ventral fin. Vent tube opening at the left side of the ventral fin, laterally concealed by spiracle, and directed downward. Caudal musculature representing 51.5% of the body height and gradually diminishing to a pointed tip. Dorsal fin originating at the tail-body junction, convex, and deeper at the middle third of the tail. Ventral fin originating at the posterior ventral terminus of the body, convex, similar throughout the anterior two-thirds of the tail but diminishing towards the tail tip. Both fins narrow abruptly to shallow fins on the terminal portion of the tail. Tail tip pointed.

Color in preservative. Body dorsum and caudal musculature dark to light brown. Body venter light brown with scarcely speckled melanophores and small white blotches. Fins translucent. Caudal musculature and fins with irregular large brown patches and small white blotches.

Variation. Variation in 17 measurements of 59 tadpoles from Gosner Stages 25–27, 31–34, 36–40, and 42–45 is given in Table 1. Total length increases gradually from Stages 25 to 39, with maximum total length observed at Stage 39 (32.49 mm). Body length and tail length averaged 38% and 62% of total length, respectively, varying from 42% and 58% at Stage 26 to 35% and 65% at Stage 39. From Stage 36 to 39 the external nares are located dorsally and consist of a rounded whitish spot. The nostril openings are visible from Stage 40 onwards. The spiracular tube is similar from Stage 25 to Stage 41. From Stage 42 onwards, spiracular tube origin is at mid-distance between hind and forelimbs with opening on the ventral surface of the body. At Stage 43, the spiracular tube is replaced by a narrow and long scar with a small opening at the midline of the ventral surface. At Stages 44 and 45, spiracular opening is not visible. The vent tube opening is medial and separated from the ventral fin from Stages 40 to 45.

The external morphology of E. helianneae tadpoles is similar to those described for other species in the genus Elachistocleis , which includes an oval body in dorsal view, a triangular/depressed body in lateral view, eyes laterally positioned, nostril openings absent, spiracle medial, long and wide, and anterior mouth with two dermal flaps ( Kenny 1969; Williams & Gudynas 1987; Kwet & Di-Bernardo 1998; Duellman 2005; Lynch 2006; Rossa-Feres & Nomura 2006; Vera Candioti 2006; Magalhães et al. 2012; Pereyra et al. 2013).

The total length of E. helianneae is similar to E. bicolor from Departamento de Maldonado, Uruguay (total length (TL) = 26.81 mm, Stage 38), E. cesarii (TL = 18.4–27.1 mm, Stages 32–34), E. erythrogaster (TL = 17.0 mm, Stage 29), and E. haroi (TL = 22.5–23.7 mm, Stage 35). Tadpoles of E. helianneae are larger than tadpoles of E. bicolor from State of São Paulo, Brazil (TL = 21.51–22.05 mm, Stages 36–38) and E. panamensis (TL = 14.57 mm, Stages 29–30), and smaller than E. muiraquitan (TL = 26.3–28.4 mm at Stage 36, 29.2–31.0 mm at Stage 37, maximum TL = 35.3 mm at Stage 39), E. ovalis and E. surinamensis (both species TL = 25.0 mm, Stage 28, information inferred from the pictures at the original paper by Kenny 1969), and Elachistocleis sp. (TL = 27.2–30.5 mm, Stage 37).

The oral dermal flaps found in the tadpoles of the genus Elachistocleis present different patterns: dermal flaps expanded with jagged edges [ E. haroi , E. panamensis , E. surinamensis , and Elachistocleis sp. (from Vitória Brasil municipality, São Paulo state, Brazil)], dermal flaps expanded without jagged edges [ E. bicolor , E. erythrogaster , E. helianneae (this study), E. pearsei , E. ovalis ], and dermal flaps short, semi-circular without jagged edges ( E. cesarii ). Information about the edges of dermal flaps for E. muiraquitan (as E. bicolor from Cusco Amazónico, Peru; Duellman 2005; Allen et al. 2014) is not available. According to Pereyra et al. (2013) this character was not clearly analyzed in some species and a thorough exploration could be important to understand the phylogeny and natural history of the genus Elachistocleis .

In addition, the tadpole of E. helianneae is distinguished from E. cesarii by the height of the fins (ventral fin is larger than dorsal fin in E. cesarii ), from E. bicolor , E. ovalis , E. pearsei , E. surinamensis , and Elachistocleis sp. by the color pattern (medial stripe on the anterior third of the tail musculature in E. bicolor and Elachistocleis sp.; color black with light stripe through eyes and along tail, irregular silver-greyish spots on body venter, and tip of the tail black in E. surinamensis ; in E. ovalis the color pattern is similar to E. surinamensis with the exception of fin pigmentation being less dense and paler in the body venter; body, caudal musculature, and fins heavily pigmented in E. pearsei ; see Figure 4 in Lynch 2006). Elachistocleis helianneae also differs from E. erythrogaster and E. muiraquitan by the origin of the dorsal fin (dorsal fin extending towards the body in E. erythrogaster ; dorsal fin originated on the tail musculature in E. muira- quitan), from E. erythrogaster , E. haroi and E. surinamensis by the tail tip pointed (tail tip rounded in E. erythrogaster , E. haroi and E. surinamensis ) and from E. panamensis by the absence of a peculiar thickening of the base of the tail and fins (present in E. panamensis ).

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We also found ontogenetic variations in spiracle and vent tube development in the tadpole of E. helianneae that is similar to those described by Lavilla & Langone (1991) in E. bicolor , in which there is a migration of the spiracular and vent tube during the climax of the metamorphosis. We observed the following exception in E. helianneae : the spiracle develops from Stages 25 to 41 and only at Stage 42 the spiracular tube was shorter with a medial opening. These observations differ from those found in E. bicolor where the spiracular tube is narrower and shorter at Stage 39 as compared with previous stages and the spiracle opening is shifted from sinistral to medial. Tadpoles of E. helianneae lose the vent tube at Stage 40, similar to E. bicolor (Lavilla & Langone 1991) and Dermatonotus muelleri (Boettger) ( Fabrezi et al. 2012) and different from Chiamoscleis lacrimae Peloso, Sturaro, Forlani, Gaucher, Mott, and Wheeler, Synapturanus mirandaribeiroi Nelson and Lescure , and Synapturanus cf. salseri Pyburn that regress the vent tube at Stage 42 ( Menin et al. 2007; Acerb Cordioli et al. 2019). The nostril openings are visible from Stage 40 in E. helianneae , earlier at Stages 38 and 39 in D. muelleri and slithgly later from Stage 41 in Chiasmocleis species ( Fabrezi et al. 2012; Acerb Cordioli et al. 2019).

Figures

FIGURE 1. Elachistocleis helianneae tadpole at Stage 36. (A) Lateral, (B) dorsal and (C) ventral views, (D) oral disc in frontal view, (E) oral disc in ventral view. Tadpole at Stage 32: (F) detail of the spiracle (sp), vent tube (vt), and hind limb (hd). CZPB-LA tadpole lot 419/886, collected at the campus of the Universidade Federal do Amapá, Macapá municipality, Amapá, Brazil.