Rhinella arenarum (Argentine toad) egg predation by leeches

MASETTI, M.C.; PEREYRA, M.O.; FAIVOVICH, J.

HERPETOLOGICAL REVIEW

Society for the Study of Amphibians and Reptiles

Año: 2015 vol. 46 p. 614 - 615

0018-084X

Leech predation on amphibians has been previously reported (Moore 1953. Not. Nat. Acad. Nat. Sci. Philadelphia 250:1-13; Cargo 1960. Chesapeake Sci. 1:119-120; Loebmann et al. 2008. Amphibia 7:31-34; Alvarez 2010. Bol. Asoc. Herpetol. Esp. 21:25-26; Tiberti and Gentilli 2010. Acta Herpetol. 5:255-258). Amphibian egg predation has been reported in North and South America, Southeast Asia, Australia, and Europe (Burgin and Schell 2005. Acta Zool. Sinica 51:349-353; Gunzburger and Travis 2005. J. Herpetol. 39:547-571; Romano and Di Cerbo 2007. Acta Zool. Sinica 53:750-754; Soler et al. 2014. Cuad. Herpetol. 28:39-41). Previous reports of anuran eggs being predated by leeches in Argentina include an unidentified Oxyptychus feeding on eggs of Rhinella dorbignyi (Dorbigny's Toad) and Hypsiboas pulchellus (Montevideo Treefrog) (Soler et al. 2014. op. cit.). Herein we report a case of egg predation on at least two clutches of Rhinella arenarum by the leech Oxyptychus striatus (Ringuelet 1945. Fauna de agua dulce de la Republica Argentina. Volumen XVII Annulata, Fasciculo 1 Hirudinea. pp. 225-232; Fig. 1). The observations were made in a very slow flowing stream in San Luis, Departamento Conlara, Ruta Provincial 5, 15 KM NW Santa Rosa del Conlara, Argentina (32.2567°S, 65.3214°W, WGS84, 717 m elev.), at ~2300 h on 19 January 2013. Several leeches (reference voucher specimens MACN-In 40169) were attached with their sucker to the gelatinous egg strings, surrounding and penetrating them with their mouths at the point where each egg was found (Fig. 2). After the eggs were consumed, the string was left completely empty (Fig. 3). Once each egg was consumed, the leech left a characteristic cylindrical projection perpendicular to the longitudinal axis of the string, as if the jelly was everted by the leech?s mouth once it finished feeding on the egg (Fig. 3).Oxyptychus is a hirudiniform genus of leeches with seven species distributed in Puerto Rico, Panama, Ecuador, and east of the Andes to the north of the extra-Andean Patagonia. Though they feed mainly on the blood of their hosts (Ringuelet 1945. op. cit.), recent observations suggest that they also prey on their eggs (Soler et al. 2014. op. cit.; present observation). Several similar cases have been observed among hirudiniforms: Macrobdella ditetra consumes blood and eggs of frogs (Moore 1953. op. cit.), and M. diplotertia has been observed attacking tadpoles and simultaneously consuming the eggs of Lithobates clamitans (Green Frog) and L. sphenocephalus (Florida Leopard Frog) (Turbeville and Briggler 2003. J. Fresh. Ecol. 18:155-159). Hirudiniform leeches of the order Arhyncobdellidae lack a proboscis, and to feed they employ their jaws to tear the skin of the host. In the case of egg predation, they manage to bypass the gelatinous capsules surrounding the eggs, perforating them with their jaws. There are different ways known to achieve this: (a) the leech Bassianobdella fusca specializes on this type of food, for which it enters the foam nest, then surrounds the egg using its ventral surface and swallows it wholly (Burgin and Schell 2005. op. cit.), and (b) M. diplotertia begins investigating the eggs with its head, and once it chooses an egg, it extends its body and secures its sucker to the gelatinous capsule of another egg to enter the selected one, and once inside, surrounds the egg and consumes it (Trauth and Neal 2004. J. Ark. Acad. Sci. 58:139-141).Most bufonids have toxins (bufadienolides) from the egg stage to adulthood. The diversity and concentration of these molecules varies during ontogeny: the eggs contain the most toxin, with toxicity decreasing during larval development and increasing again after metamorphosis. The surrounding jelly coat that protects the eggs from predators lacks these toxins (Hayes et al. 2009. J. Chem. Ecol. 35:391-399). In Australia, deaths of native species of turtles and fish were reported after consuming eggs of Rhinella marina and, to a lesser extent, its tadpoles (Greenlees and Shine 2011. Austral Ecol. 36:53-58). Insects can also find the early stages of toads unpalatable: cases where Odonata larvae preferred not to consume tadpoles of R. spinulosa papillosa have been recorded (Jara and Perotti 2006. Cuad. Herpetol. 19:37-42). In contrast, Dytiscidae beetles prefer R. marina tadpoles to native Australian tadpoles or fish (Cabrera-Guzmán et al. 2012. Biol. Cons. 153:1-9). However, there are reports of leeches that apparently are not affected by these toxins and consume eggs and tadpoles of bufonids (see revisions of Gunzburger and Travis 2005. op. cit.; Romano and di Cerbo 2007. op. cit.). Nevertheless, there are also cases where other species of leeches have been affected by these toxins, such as Goddardobdella elegans where the survival rate was significantly reduced after feeding on tadpoles of R. marina (Crossland and Alford 1998. Aust. J. Ecol. 23:129-137). In that same study, other invertebrates did not suffer lethal effects after consuming eggs or tadpoles. Litch (1969. Am. Midl. Nat. 82:296-298) also reported unpalability of eggs of Anaxyrus boreas by Haemopsis sp., showing a high aversion to egg compounds.Leeches of the genus Oxyptychus are likely natural predators of Rhinella. The specific mechanism that allows these leeches to tolerate the toxicity of egg compounds so that they may be consumed safely is unknown.