Herpetology Notes, volume 14: 799-801 (2021) (published online on 19 May 2021)

Necrophilic behaviour of Amazophrynella teko in northern

Carlos Eduardo Costa-Campos1,*, Marcos Roberto Dias-Souza2, and Antoine Fouquet3

Frogs display a wide variety of reproductive modes males much smaller than females (snout–vent length (e.g., Haddad and Prado, 2005; Wells, 2007) that have in males 12.9–15.8 mm vs. 17.9–21.5 mm in females; produced a bewildering array of sexual interactions Rojas et al., 2018). Amazophrynella species display (e.g., Simović et al., 2014; Berneck et al., 2017). the same reproductive mode that predominates in the Among the more unusual of these is necrophilic family Bufonidae, consisting of egg deposition in behaviour, which has been reported in several lentic or lotic water with exotrophic tadpoles (Haddad families, including Bombinatoridae (Sinovas, 2009), and Prado, 2005; Menin et al., 2014, 2020). Here, we Bufonidae (Marco and Lizana, 2002; Ayres, 2010; provide the first observation of necrophilic behaviour Alvarez, 2011; Brito et al., 2012; Izzo et al., 2012; in A. teko, which is also the first report for the genus Patel et al., 2016), Hylidae (Bedoya et al., 2014; Moura Amazophrynella. and Loebmann, 2014), Leptodactylidae (Lemos and The observation took place on 24 March 2019 at Lourenço-de Moraes, 2019), and Ranidae (Pearl et al., ca. 18:40 h, when an amplectant pair of A. teko was 2005; Bettaso et al., 2008; Garwood and Anderson, discovered in Colônia de Água Branca, Serra do 2010; Groffen et al., 2019). This behaviour seems to Navio Municipality, Amapá State, northern Brazil be most commonly observed in explosive-breeding (0.9429°N, 51.9438°W). The male (SVL = 14.0 species, in which females may die due to the aggressive mm) was observed in axillary amplexus with a dead nature of the interactions with other individuals, but it conspecific female (SVL = 20.0 mm) in the leaf litter of also occurs in a few species with prolonged breeding a primary forest, near rain-filled water bodies (Fig. 1). periods (Groffen et al., 2019). Several egg clutches were seen in a nearby temporary Amazophrynella teko Rojas et al., 2018 is a small pond, and calling males were heard in the vicinity, species distributed in French Guiana, Amapá State of indicating ongoing reproductive activity. The pair was Brazil, and in the southern region of Suriname (Rojas collected, and the specimens have been deposited in et al., 2018). The species is diurnal and crepuscular, the Herpetological Collection, Universidade Federal but it is also active at night during its peak breeding do Amapá (CECC 2902–03). period, which normally occurs in a short time period at Necrophilic behaviour has been reported for several the beginning of the rainy season (Rojas et al., 2018). explosive-breeding (Bufo bufo – Marco and A marked sexual dimorphism exists in A. teko, with Lizana, 2002; jimi – Brito et al., 2012; R. proboscidea – Izzo et al., 2012; Duttaphrynus melanostictus – Patel et al., 2016). These species display what we consider the “range-expansion 1 Laboratório de Herpetologia, Departamento de Ciências phenotype” (i.e., large body size, skin resistant to Biológicas e da Saúde, Universidade Federal do Amapá, drying out, parotoid glands, inguinal fat bodies, Rodovia JK, Km 2, Macapá, Amapá, 68903-499, Brazil. and an ability to lay large numbers of eggs in 2 Laboratório de Biologia Celular e Helmintologia “Prof. Dra diverse environments), which probably fostered the Reinalda Marisa Lanfredi”, Instituto de Ciências Biológicas, diversification and the dispersal of these bufonids Universidade Federal do Pará, Belém, Pará 66075-110, Brazil. (Van Bocxlaer et al., 2010). Our report is the first of 3 Laboratoire Evolution et Diversité Biologique, UMR5174, necrophilia for the genus Amazophrynella and suggest Bâtiment 4R1, 118 Route de Narbonne, 31062 Toulouse that necrophilic behaviour may be more widespread in Cedex 9, France. toads than expected, given that A. teko is not a typical * Corresponding author. E-mail: [email protected] “range-expansion” species. © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. Studies have reported that males can accidentally 800 Carlos Eduardo Costa-Campos et al.

Figure 1. Necrophilia in Amazophrynella teko in the leaf litter near rain-filled water bodies in a primary forest in Amapá State, northern Brazil. The male is alive, continuing to perform axillary amplexus, even though his partner has died. Photograph by Carlos Eduardo Costa-Campos. drown females during the intense, frenetic mating revisions on our manuscript, and Instituto Chico Mendes de activity of explosive-breeding species (e.g., Davies Conservação da Biodiversidade (ICMBio, #48102-2) for the and Halliday, 1979; Wells, 2007; Izzo et al., 2012). collection permit. While such reproductive frenzies may appear costly References from a point of natural selection by likely denying successful mating to both members of a pair with a Alvarez, J.A. (2011): Natural history notes. Bufo boreas (Western drowned partner, they may simultaneously foster Toad). Davian behavior. Herpetological Review 42: 408–409. selective pressures that favour stronger and more Ayres, C. (2010): Natural history notes. Bufo bufo (Common Toad). Davian behavior. Herpetological Review 41: 192–193. persistent members of both sex (Izzo et al., 2012). Even Bedoya, S.C., Mantilla-Castaño, J.C., Pareja-Márquez, I.M. (2014): if survival of the female is not possible, the pressure Necrophiliac and interspecific amplexus in Dendropsophus of the amplectant male on a recently deceased female columbianus (Anura: Hylidae) in the Central Cordillera of may still result in successful ejection of viable oocytes . Herpetology Notes 7: 515–516. and fertilization, as seen in (Izzo Berneck, B.V.M., Segalla, M.V., Haddad, C.F.B. (2017): A first et al., 2012). This may then be an extreme form of a observation of amplexus in Aplastodiscus (Anura; Hylidae). “functional strategy” that could minimize losses to both Herpetology Notes 10: 351–354. Bettaso, J., Haggarty, A., Russell, E. (2008). Natural history partners in terms of mating success during explosive- notes. Rana boylii (Foothill Yellow-legged Frog). Necrogamy. breeding events. Unfortunately, we were unable to Herpetological Review 39: 462. confirm whether the male of A. teko amplecting the Brito, L.B.M., Joventino, I.R., Ribeiro, S.C., Cascon, P. (2012): dead female had successfully fertilized her eggs. Necrophiliac behavior in the “cururu” toad, Stevaux, 2002, (Anura, Bufonidae) from northeastern Brazil. Acknowledgements. The authors would like to thank Philippe North-Western Journal of Zoology 8: 365–366. Kok and Hinrich Kaiser for the constructive feedback and Davies, N.B., Halliday, T.R. (1979): Competitive mate searching Necrophilic Behaviour of Amazophrynella teko 801

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Accepted by Hinrich Kaiser