death and life on the roadway: scavenging behaviour of the

3
Roads may have direct and indirect negative effects on wildlife and pose significant threat to vertebrates at the global level (Forman et al., 2003). Besides causing direct mortality, roads may have other impacts including the partial occupation and transformation of landscapes, alteration of surrounding habitats, dispersal of physicochemical pollutants, habitat fragmentation and they may reduce habitat connectivity (Forman et al., 2003; Colino-Rabanal and Lizana, 2012). The mortality rate of animals on roads may depend on season, traffic density and the behaviour of species involved (Bhupathy et al., 2011). Carcasses of road killed animals can be removed and consumed by scavengers (Gillingham and Baker, 1981; Antworth et al., 2005). The scavenging behaviour of snakes not associated with road killed animals has been widely reported worldwide (see review by De Vault and Krochmal, 2002; Marques et al., 2017), based on observations of carrion consumption in situ (e.g. Paten and Banta, 1980; Sazima and Strüssmann, 1990; Otto and Miller, 2004; Trembath et al., 2007; Platt and Rainwater, 2011; Sweeting, 2011; Ayres, 2012) and in captivity (Gillingham and Baker, 1981; Shivik and Clark, 1997), from the examination of stomach contents (Capula et al., 1997), and presentation of dead prey items during staged encounters (Sazima and Strüssmann, 1990; Marques and Sazima, 1997). Herein, we report for the first time the scavenging behaviour of the Neotropical green racer snake Philodryas patagoniensis (Girard, 1858) (Dipsadidae), a species typical of open areas such as savannahs and grasslands (Marques et al., 2001; Giraudo, 2004; López and Giraudo, 2008) of Argentina, Bolivia, Brazil, Paraguay, and Uruguay (Uetz and Hošek, 2016). P. patagoniensis is a terrestrial snake (Sazima and Haddad, 1992; Marques et al., 2001) and is considered a generalist predator of small invertebrates, small vertebrates, as well as cannibalistic species (Hartmann and Marques, 2005; Lopes and Giraudo, 2008; Carreira and Maneyro, 2013). Our observations were made during field activities of our roadkill monitoring project on 07 November 2015, at km 355 (30°47’ 33”S, 55°39’42”W, 318m a.s.l.) of BR 293 Road, which crosses the “Área de Proteção Ambiental do Ibiratpuitã” – the largest conservation unit in the Pampa Biome - in the municipality of Santana do Livramento, Rio Grande do Sul State, Brazil. At approximately 15:30 h we observed an adult P. patagoniensis (total length ca. 100 cm) on the asphalt that then proceeded to remove a dead rufous hornero (Furnarius rufus, Furnariidae) from the centre of road (Fig.1). The dead bird presented visible rigor mortis, flattened body, partially open wings and scruffy plumage. The snake moved from the road edge, gripping the dead bird by the head. The snake carried the carcass (lifted off the ground) from the asphalt to the grassy vegetation by the roadside when approached by one of the authors (J.U.), the snake then attempted to swallow the bird (Fig. 1). The observation lasted approximately 20 min, after which the snake moved into dense vegetation. Scavenging by snakes has been traditionally discounted or ignored (De Vault and Krochmal, 2002), and most records in the Neotropical region include in situ observations or staged encounters (not carcass removal from roadways) (see Sazima and Strüssmann, 1990; Marques and Sazima, 1997; Marques et al. 2017): Helicops modestus, Hydrodynastes gigas, Erythrolamprus miliaris, Bothrops jararaca, Micrurus corallinus and M. frontalis. Indeed, carcass removal from roadways has been reported in at least six snake species around the world; a rattlesnake (Crotalus ruber) which was recorded eating a rodent in the USA (Patten Herpetology Notes, volume 10: 439-441 (2017) (published online on 25 August 2017) Death and life on the roadway: scavenging behaviour of the green racer snake Philodryas patagoniensis (Girard, 1858) (Dipsadidae) João Ucha 1 and Tiago G. dos Santos 1, * 1 Universidade Federal do Pampa, Campus São Gabriel. Av. Antônio Trilha, 1847. CEP: 97300-000. São Gabriel, Rio Grande do Sul state, Brazil * Corresponding author: [email protected]

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Page 1: Death and life on the roadway: scavenging behaviour of the

Roads may have direct and indirect negative effects on wildlife and pose significant threat to vertebrates at the global level (Forman et al., 2003). Besides causing direct mortality, roads may have other impacts including the partial occupation and transformation of landscapes, alteration of surrounding habitats, dispersal of physicochemical pollutants, habitat fragmentation and they may reduce habitat connectivity (Forman et al., 2003; Colino-Rabanal and Lizana, 2012). The mortality rate of animals on roads may depend on season, traffic density and the behaviour of species involved (Bhupathy et al., 2011). Carcasses of road killed animals can be removed and consumed by scavengers (Gillingham and Baker, 1981; Antworth et al., 2005). The scavenging behaviour of snakes not associated with road killed animals has been widely reported worldwide (see review by De Vault and Krochmal, 2002; Marques et al., 2017), based on observations of carrion consumption in situ (e.g. Paten and Banta, 1980; Sazima and Strüssmann, 1990; Otto and Miller, 2004; Trembath et al., 2007; Platt and Rainwater, 2011; Sweeting, 2011; Ayres, 2012) and in captivity (Gillingham and Baker, 1981; Shivik and Clark, 1997), from the examination of stomach contents (Capula et al., 1997), and presentation of dead prey items during staged encounters (Sazima and Strüssmann, 1990; Marques and Sazima, 1997).

Herein, we report for the first time the scavenging behaviour of the Neotropical green racer snake Philodryas patagoniensis (Girard, 1858) (Dipsadidae), a species typical of open areas such as savannahs and grasslands (Marques et al., 2001; Giraudo, 2004; López and Giraudo, 2008) of Argentina, Bolivia, Brazil,

Paraguay, and Uruguay (Uetz and Hošek, 2016). P. patagoniensis is a terrestrial snake (Sazima and Haddad, 1992; Marques et al., 2001) and is considered a generalist predator of small invertebrates, small vertebrates, as well as cannibalistic species (Hartmann and Marques, 2005; Lopes and Giraudo, 2008; Carreira and Maneyro, 2013). Our observations were made during field activities of our roadkill monitoring project on 07 November 2015, at km 355 (30°47’ 33”S, 55°39’42”W, 318m a.s.l.) of BR 293 Road, which crosses the “Área de Proteção Ambiental do Ibiratpuitã” – the largest conservation unit in the Pampa Biome - in the municipality of Santana do Livramento, Rio Grande do Sul State, Brazil. At approximately 15:30 h we observed an adult P. patagoniensis (total length ca. 100 cm) on the asphalt that then proceeded to remove a dead rufous hornero (Furnarius rufus, Furnariidae) from the centre of road (Fig.1). The dead bird presented visible rigor mortis, flattened body, partially open wings and scruffy plumage. The snake moved from the road edge, gripping the dead bird by the head. The snake carried the carcass (lifted off the ground) from the asphalt to the grassy vegetation by the roadside when approached by one of the authors (J.U.), the snake then attempted to swallow the bird (Fig. 1). The observation lasted approximately 20 min, after which the snake moved into dense vegetation.

Scavenging by snakes has been traditionally discounted or ignored (De Vault and Krochmal, 2002), and most records in the Neotropical region include in situ observations or staged encounters (not carcass removal from roadways) (see Sazima and Strüssmann, 1990; Marques and Sazima, 1997; Marques et al. 2017): Helicops modestus, Hydrodynastes gigas, Erythrolamprus miliaris, Bothrops jararaca, Micrurus corallinus and M. frontalis. Indeed, carcass removal from roadways has been reported in at least six snake species around the world; a rattlesnake (Crotalus ruber) which was recorded eating a rodent in the USA (Patten

Herpetology Notes, volume 10: 439-441 (2017) (published online on 25 August 2017)

Death and life on the roadway: scavenging behaviour of the green racer snake Philodryas patagoniensis (Girard, 1858)

(Dipsadidae)

João Ucha1 and Tiago G. dos Santos1,*

1 Universidade Federal do Pampa, Campus São Gabriel. Av. Antônio Trilha, 1847. CEP: 97300-000. São Gabriel, Rio Grande do Sul state, Brazil

* Corresponding author: [email protected]

Page 2: Death and life on the roadway: scavenging behaviour of the

João Ucha & Tiago G. dos Santos440

and Banta, 1980), a banded cat-eyed snake (Leptodeira annulata) eating a road killed frog in Costa Rica (Mora-Benavides, 1999), a Cape cobra (Naja nivea) scavenging on snakes in South Africa (Phelps, 2006), a python (Antaresia childreni) scavenging on a lizard

in Australia (Trembath et al., 2007), a Montpellier snake (Malpolon monspessulanus) scavenging on a bird in Spain (Ventura, 2012) and the Common Kukri snake (Oligodon arnensis) scavenging on a lizard in India (Pandirkar et al., 2015). Aquatic or semi-aquatic

Figure 1. Schematic summary of an adult of Philodryas patagoniensis carrying the carcass of Furnarius rufus after removing it from BR 293 Road, Conservation Unit “Área de Proteção Ambiental do Ibiratpuitã”, municipality of Santana do Livramento, state of Rio Grande do Sul, Brazil.(1) Location of the dead bird on the road; (2) initial location of the snake when it was seen, and (3) point where the snake attempted to swallow the bird.

Page 3: Death and life on the roadway: scavenging behaviour of the

piscivorous snake species are more often observed scavenging than arboreal or predominantly terrestrial species (Sazima and Strüssmann, 1990), such as P. patagoniensis. Roadways can be a predictable food source for snakes (De Vault and Krochmal, 2002), and further studies on the subject are needed since scavengers can bias estimates of road-killed vertebrates. Moreover, if widespread and recurrent, scavenging behaviour can be an underestimated cause of snake mortality on roads.

Acknowledgements. TGS thanks the National Council for Scientific and Technological Development (CNPq) for the research fellowship (process #307352/2013-7). We are grateful to anonymous reviewers and Editor for the comments and suggestions on the manuscript.

References

Antworth, R.L., Pike, D.A., Stevens, E.E. (2005): Hit and run: effects of scavenging on estimates of roadkilled vertebrates. Southeastern Naturalist 4: 647–656.

Ayres, C. (2012): Scavenging in the genus Natrix. Acta Herpetologica 7: 171–174.

Bedford, G. (1991): Record of road kill predation by the fresh water snake (Tropidonophis mairii). Herpetofauna 21: 35–36.

Bhupathy, S., Rinivas, G., Kumar, N.S., Karthik, T., Madhivanan, A. (2011): Herpetofaunal mortality due to vehicular traffic in the western Ghats, India: A case study. Herpetotropicos 5:119–126.

Capula, M., Luiselli, L., Rugiero, L., Evangelisti, F., Anibaldi, C., Jesús, V.T. (1997): Notes on the food habits of Coluber hippocrepis nigrescens from Pantelleria Island: a snake that feeds on both carrion and living prey. Herpetological Journal 7: 67–70.

Carreira, S., Maneyro, R. (2013): Guía de Reptiles Del Uruguay. Ediciones de la Fuga, Montevideo.

Colino-Rabanal, V.J., Lizana, M. (2012): Herpetofauna and roads: a review. Basic and Applied Herpetology 26:5–31.–31.

Devault, T.L., Krochmal, A.R. (2002): Scavenging by snakes: an examination of the literature. Herpetologica 58: 429–436.

Forman, R.T.T., Sperling, D., Bissonette, J.A., Clevenger, A.P., Cutshall, C.D., Dale, V.H., Fahrig, L., France, R., Goldman, C.R., Heanue, K., Jones, J.A., Swanson, F.J., Turrentine, T., Winter, T.C. (2003): Road Ecology. Island Press, Washington DC.

Gillingham, J.C., Baker, R.E. (1981): Evidence for scavenging behavior in the Western Diamond Back Rattlesnake (Crotalus atrox). Zeitschrift fur Tierpsychologie 55: 217–227.–227.

Giraudo, A.R. (2004): Serpientes de la selva Paranaense y del Chaco Húmedo.L.O.L.A., Buenos Aires.

Hartmann, P.A., Marques, O.A.V. (2005): Diet and habitat use of two sympatric species of Philodryas (Colubridae), in south Brazil. Amphibia-Reptilia 26: 25–31.

López, M.S., Giraudo, A.S. (2008): Ecology of the snake Philodryas patagoniensis (Serpentes, Colubridae) from Northeast Argentina. Journal of Herpetology 42: 474–480.

Marques, O.A.V., Eterovic, A., Sazima, I. (2001): Serpentes da Mata Atlântica: Guia Ilustrado para a Serra do Mar. Editora Holos, Ribeirão Preto.

Marques, O.A.V., Coeti, R.Z., Braga, P.A., Sazima, I. (2017): Rotten choice: feeding attempt by a coral snake (Micrurus frontalis) on a dead pitviper (Bothrops jararaca) that had swallowed a bulky rodent. Herpetology Notes 5: 137–139.

Marques, O.A.V., Sazima, I. (1997): Diet and feeding behavior of the coral snake, Micrurus corallinus, from the Atlantic Forest of Brazil. Herpetological Natural History 5: 88–93.

Mora-Benavides, J.M. (1999): Leptodeira annulata (Culebra Destenida, Banded Cat-eyed Snake): Diet. HerpetologicalReview 30: 102.

Otto, C.R., Miller, G.J. (2004): Philodryas viridissimus (Green Palm Snake). Feeding attempt. Herpetological Review 35: 277.

Pandirkar, A., Karve, H., Ghadigaonkar, P., Todankar, R., Kuwar, A., Jangam, P., Bandekar, P., Mahangade, A. (2015): First record of scavenging by Oligodon arnensis (Shaw, 1802) from Tungareshwar Wildlife Sanctuary, India. Reptile Rap 17:19–21.

Patten, R.B., Banta, B.H. (1980): A rattlesnake Crotalus ruber feeds on a road-killed animal. Journal of Herpetology 14: 111–112.

Platt, S.G., Rainwater, T.R. (2011): An observation of scavenging by Crotalus molossus (Baird and Girard, 1853). Journal of Kansas Herpetology 37: 8–9.

Phelps, T. 2006. Naja nivea (Linnaeus, 1758) Cape cobra. Scavenging. African Herpetological News 40: 24.

Sazima, I., Haddad, C.F.B. (1992): Répteis da Serra do Japi. Notas sobre história natural. In: História Natural da Serra do Japi. Ecologia e Preservação de uma área florestal no sudeste do Brasil, pp. 212–23. Morellato, L.P.C., Ed., Editora Unicamp, Campinas.

Sazima, I., Strüssmann, C. (1990): Necrofagia em serpentes brasileiras: exemplos e previsões. Revista Brasileira de Biologia50: 461–468.

Shivik, J.A., Clark, L. (1997): Carrion seeking in brown tree snakes: importance of olfactory and visual cues. Journal Experimental Zoology 279: 549–553.

Sweeting, T. (2011): Vipera berus (adder): Feeding. Herpetological Bulletin 116: 31.

Trembath, D.F., Blackburn III, J.L., Rowley, J.J.L. (2007): Road kill predation by a Children’s Python Antaresia children (Serpentes: Boidae) at Adelaide River, Northern Territory. Northern Territory Naturalist 19: 58–59.

Uetz, P., Hošek, J. (2016): Philodryas patagoniensis. The Reptile Database. Available at: http://www.reptile-database.org. Accessed on 17 July 2016.

Ventura, F. (2012): Comportamiento carroñero en Malpolon monspessulanus. Boletín de la Asociación Herpetológica Española 23:8–10.

Death and life on the roadway: scavenging behaviour of Philodryas patagoniensis 441

Accepted by Benjamin Tapley