Confirming Domergue: Ithycyphus oursi Domergue, 1986 predation upon Furcifer oustaleti (Mocquard, 1894)

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1 Herpetology Notes, volume 3: (2010) (published online on 5 May 2010) Confirming Domergue: Ithycyphus oursi Domergue, 1986 predation upon Furcifer oustaleti (Mocquard, 1894) Angelica Crottini 1,2, *, D. James Harris 3, Iker A. Irisarri 4, Alexandra Lima 3,5, Solohery Rasamison 6, Gonçalo M. Rosa 7 Abstract. We report on one individual of the Malagasy endemic snake Ithycyphus oursi predating upon a female of Furcifer oustaleti at Isalo National Park, central-southern Madagascar. Although known from the close Zombitse and Vohibasia forests, this is also the first record of this colubrid snake in the Isalo Massif. Keywords. Madagascar, Isalo, Serpentes, Chamaeleonidae, predation, arboreal, diet. About 75 species of colubrid snakes, grouped in 18 genera, are currently known from Madagascar, although several still await formal description (Cadle 2003; Glaw, Vences 2007). Systematics and phylogenetic relationships are still poorly known, but almost all Malagasy colubrids belong to a single radiation, named the Pseudoxyrhophiinae, recently included in the family Elapidae (Lawson, Slowinski, Burbrink 2004) or the Lamprophiidae (Vidal et al. 2007). Most of the genera and all species are endemic to Madagascar (Raxworthy 2003; Glaw, Vences 2007). Life history aspects of 1 Division of Evolutionary Biology, Zoological Institute, Technical University of Braunschweig, Spielmannstr. 8, 38106, Braunschweig, Germany; tiliquait@yahoo.it 2 Universitá degli Studi di Milano, Dipartimento di Biologia, Sezione di Zoologia e Citologia, Via Celoria 26, Milano, Italy; 3 CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, Vairão, Portugal; 4 Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales (CSIC), José Gutiérrez Abascal 2, Madrid, Spain; 5 Departamento de Zoologia-Antropologia, Facultade de Ciências da Universidade do Porto, Porto, Portugal; 6 Université d Antananarivo, Faculté des Sciences, Département de Biologie Animale; 7 Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, Portugal. *corresponding author Malagasy snakes are largely unknown, although very important to fully understand the ecology of the species. While trophic ecology of mainland African snakes is fairly well known, only scattered data are available for Malagasy snakes (Preston-Mafham 1991; Cadle 1996a, 1996b; Vences et al. 2004, Mercurio et al. 2006; Glaw, Vences 2007; Knoll, Glaw, Köhler 2009). The prey items of Malagasy colubrids mostly consist of frogs and lizards, but also ophiophagous and opportunistic egg-eating snakes have been reported (Domergue 1987; Preston-Mafham 1991; Mercurio et al. 2006; Knoll, Glaw, Köhler 2009). The genus Ithycyphus comprises five diurnal, mediumsized and arboreal Madagascan colubrid species (Glaw, Vences 2007). These species are generally considered calm and reluctant to bite, even when handled (Mori, Mizuta 2006). They have opisthoglyphous dentition and mild envenomation is known (Domergue 1986; Mori, Mizuta 2006). Domergue (1986) reported on a Furcifer lateralis seized and paralyzed in about two minutes by an Ithycyphus oursi held in captivity. The secretions from Duvernoy s glands is known to be responsible for the pharmacological effects caused by a bite of snakes of the genus Madagascarophis (Domergue 1989), and Mori and Mizuta (2006) postulate on the likely presence of these glands also in snakes of the genus Ithycyphus, although no explicit description of these glands is available (McKinstry 1983). Ithycyphus oursi inhabits arid forests of the southerneast part of the island and it is not an easy species to spot due to its low population densities and cryptic

2 128 Angelica Crottini et al. Figure 1. An individual of Ithycyphus oursi predating upon a female Furcifer oustaleti in Namaza, Isalo NP, Madagascar, on 7th December 2009: (A-B) snake attacking and fighting with the chameleon; (C-E) snake biting the already immobilized chameleon on its dorsum; (F) the snake s first failed attempt at swallowing the prey. Photos by Gonçalo M. Rosa. nature (Glaw, Vences 2007; D Cruze et al., 2009). Little is known regarding its diet, and so far only Furcifer oustaleti has been reported as prey in the wild, having been found in the stomach content of the paratype male 1039/S (Domergue 1986). During our ongoing research work on the herpetofauna of the Isalo Massif, on 7th December 2009, an individual of I. oursi (body length ±120cm) was observed in Isalo National Park, central-southern Madagascar (Fianarantsoa Province, Antsohy Fivondronona, Ranohira Firaisana), at Namaza Valley ( S; E, 765 m a.s.l.) preying on a female of Furcifer oustaleti. The air temperature was 22 C, and the humidity of the air was 75%. The snake and the chameleon were observed fighting on the ground of the forest. When the authors approach the animals (at 17:04), the chameleon was alive, and for about 2 minutes was still moving and biting the snake, while the snake was also biting and subduing it (Fig. 1A, B). The snake firmly seized the chameleon and deeply embedded its enlarged maxillary teeth into the posterior dorsum (Fig. 1C-E). After some minutes,

3 Ithycyphus oursi predation upon Furcifer oustaleti 129 Figure 2. An individual of Ithycyphus oursi predating upon a female Furcifer oustaleti in Namaza, Isalo NP, Madagascar, on 7th December 2009: (A) snake loosening its grip on the dead prey; (B-F) the snake started swallowing its prey from the head. Photos by Gonçalo M. Rosa. similar to the case reported by Domergue (1986), the chameleon was paralyzed and a dark patch appeared on the flanks, probably caused by internal bleeding, where the snake was biting (Fig. 1E-F). The snake maintained its firm grasp, repeating chewing motions several times for approximately two minutes. Following the bite, the snake made its first failed attempt at swallowing, starting from the hind limbs (Fig. 1F), but after several attempts it loosened its grip on the dead prey. Gently holding the Furcifer oustaleti, the snake paused for approximately 60 seconds (Fig. 2A). About 25 minutes after the capture, the snake finally started swallowing its prey from the head (Fig. 2B-F; Fig. 3). It took about 44 minutes until the tip of the chameleons tail was completely inside the snake s mouth (Fig. 2B-F; Fig. 3A-F). Domergue (1986) reported that the swallowing of a Furcifer lateralis started from the hindlimbs and lasted for three minutes. The behaviour we report (killing and swallowing) lasted for about 1 hour and 10 minutes, probably due to the larger dimension of a female of F. oustaleti, with respect to an individual of F. lateralis. In fact, F. oustaleti is one of the largest chameleon species

4 130 Angelica Crottini et al. Figure 3. An individual of Ithycyphus oursi predating upon a female Furcifer oustaleti in Namaza, Isalo NP, Madagascar, on 7th December 2009: (A-E) snake swallowing the chameleon starting from its head until the tip of the chameleon s tail is completely inside the snake s mouth; (E) maxillary movements allowing the distension required by the passage of the prey; (F) snake resting after eating the chameleon. Photos by Gonçalo M. Rosa. of the world, whose females can reach a total length of about 400mm while those of F. lateralis generally have half of that body length (about 230mm) (Glaw and Vences 2007). Tissue sample of both animals have been collected for genetic analyses (Ithycyphus oursi: ACZC 1932; Furcifer oustaleti: ACZC 1929). Ithycyphus oursi is already known from ZombitseVohibasia National Park, about 90 km west of the Isalo Massif, between Sakaraha and Maninday. The forests of Vohibasia and Zombitse are considered a transition between the dry and wet forest of Madagascar, and they typically host dense decidous forest and xerophilous bushland, while in Isalo this species has been found in secondary forest along a permanent watercourse. The present observation is the first fully documented record of predation upon F. oustaleti by I. oursi in nature and it is the first occurrence record of Ithycyphus oursi for the Isalo Massif.

5 Ithycyphus oursi predation upon Furcifer oustaleti Acknowledgements. For help in the field, we are indebted to our guides Emile Rajeriarison and Bonne Année. The work was carried out in collaboration with the Département de Biologie Animale, Università d Antananarivo (UADBA), and the Association Nationale pour la Gestion des Aires Protégées (ANGAP). We are grateful to Franco Andreone, Miguel Vences and the Malagasy authorities, in particular the Ministère de l Environnement et des Eaux et Forêts, for research permits. Fieldwork was partially funded by FCT (PTDC/BIA-BDE/65745/2006) and A. Lima holds a PhD grant (SFRH/BF/47438/2008) funded by Fundação para Ciência e Tecnologia (FCT), Portugal. References Cadle, J.E. (1996a): Snakes of the genus Liopholidophis (Colubridae) from eastern Madagascar: New species, revisionary notes, and an estimate of phylogeny. Bull. Mus. Comp. Zool. 154: Cadle, J.E. (1996b): Snakes of the genus Geodipsas (Colubridae) from Madagascar, with descriptions of new species and observations on natural history. Bull. Mus. Comp. Zool. 155: Cadle, J.E. (2003): Colubridae, Snakes. In: The Natural History of Madagascar, pp Goodman, S.M., Benstead, J.P., Eds., University of Chicago Press, Chicago and London. D Cruze. N., Olsonn, A., Henson, D., Kumar, S., Emmett, D. (2009): The Amphibians and Reptiles of the lower Onilahy river valley, a temporary protected area in Southwest Madagascar. Herp. Cons. Biol. 4: Domergue, C.A. (1986): Notes sur les serpents de la région malgache VI. Le genre Ithycyphus Günther, 1973; description de deux espéces nouvelles. Bull. Mus. Nat. Hist. Nat., Paris, Ser. 4, Sec. A. 8: Domergue, C.A. (1987): Notes sur les serpents de la région malgache VII. Révision du genre Madagascarophis MERTENS, Bull. Mus. Nat. Hist. Nat., Paris, Ser. 4, 9: Domergue, C.A. (1989): Un serpent venimeux de Madagascar. Observation de deux cas de morsure par Madagascarophis (Colubridé opisthoglyphe). Arch. Inst. Pasteur Madagascar, 56: Glaw, F., Vences, V. (2007): A Field Guide to the Amphibians and Reptiles of Madagascar. Third Edition. Köln, Vences & Glaw, 496 pp. McKinstry, D.M. (1983): Morphologic evidence of toxic saliva in colubrid snakes: a checklist of world genera. Herp. Rev. 14: Mercurio, V., Mattioli, F., Razafindrabe, T.J., Andreone, F. (2006): A possible attempt of predation of Liophidium vaillanti upon Dromicodryas bernieri observed in central-southern Madagascar (Serpentes: Colubridae). Salamandra 42: Mori, A., Mizuta, T. (2006): Envenomation by the Madagascan colubrid snake Ithycyphus miniatus. J. Venom. Anim. Toxins incl. Trop. Dis. 12: Lawson, R., Slowinski, J.B., Burbrink, F.T. (2004): A molecular approach to discerning the phylogenetic placement of the enigmatic snake Xenophidion schaeferi among the Alethinophidia. J. Zool. 263: Preston-Mafham, K. (1991): Madagascar: A Natural History. Oxford (Facts on File), 224 pp. Raxworthy, C.J. (2003): Introduction to the reptiles. In: The Natural History of Madagascar, pp Goodman, S.M., Benstead, J.P., Eds., University of Chicago Press, Chicago and London. Vences, M., Glaw, F., Mercurio, V., Andreone, F. (2004): Review of the Malagasy tree snakes of the genus Stenophis (Colubridae). Salamandra 40: Vidal, N., Delmas, A.S., David, P., Cruaud, C., Couloux, A., Hedges, B. (2007): The phylogeny and classification of caenophidian snakes inferred from seven nuclear protein-coding genes. Compt. Rend. Soc. Biol. 330: Accepted by Miguel Vences

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ENVENOMATION BY THE MALAGASY COLUBRID SNAKE Langaha madagascariensis D CRUZE NC (1)

ENVENOMATION BY THE MALAGASY COLUBRID SNAKE Langaha madagascariensis D CRUZE NC (1) Received: January 28, 2008 Accepted: May 26, 2008 Abstract published online: May 30, 2008 Full paper published online: August 31, 2008 J. Venom. Anim. Toxins incl. Trop. Dis. V.14, n.3, p.546-551, 2008.