3
The red swamp crayfish, Procambarus clarkii, is native from northern Mexico and south-central United States (Hobbs Jr., 1989). The species was introduced in several countries for aquaculture or to be used as a pet. Currently, its distribution comprises all the continents, except Australia and Antarctica (Huner, 1977). In Brazil the first report of its occurrence dates from the 1980’s, when the species could be found for sale in pet shops (Magalhães et al., 2005). The introductions of the red crayfish on Latin America were motivated by the demand of United States’ market, where it is consumed (Hobbs III et al., 1989). In São Paulo State, southeastern Brazil, however, the species was most likely introduced to be used as pet, being dispersed throughout many water bodies in the region due to intentional or accidental release by aquarium keepers. Nowadays, P. clarkii can be found in the eastern São Paulo (Magalhães et al., 2005). Rhinella ornata is a medium-sized frog that belongs to the family Bufonidae. It is a nocturnal and abundant species, found in open or forested areas in southeastern Brazil (Haddad et al., 2008). These toads are very well adapted to inhabit anthropized habitats (Baldissera, 2010). On 15 August, 2012, during field work at night, two events of predation of R. ornata by P. clarkii were observed around 10:40 pm, in a swamp located at Lymington Foundation (23.96478ºS 047.01452ºW), a reserve of Atlantic Forest, Juquitiba, São Paulo. One specimen of R. ornata was being attacked by four crayfishes, each of them clinging on a toad’s leg. When we approached, the toad and the crayfishes ran away. Another individual of this frog was being preyed by two crayfishes (Fig. 1). At this time, we captured the toad during the event of predation, and it showed lacerations on the abdomen and femoral musculature, as well as amputated feet (Fig. 2). Reports on predation of R. ornata by invertebrates are already available in the literature, and, as seen now, it concurred with a reproductive explosion of the toads, when the males search actively for the females in water bodies (Haddad and Bastos, 1997). Concerning the actual predator, P. clarkii, it has caused impact on the native fauna of several regions in the world, as shown in the following examples. This crustacean is the vector of the fungus Austrapotamobius pallipes, which causes the reduction of native crayfish species, such as the European crayfish Aphanomyces astaci (Gil-Sánchez and Alba-Tercedor, 2001). It has been already reported that P. clarkii may also cause high mortalities in amphibians (Cruz et al., 2006). The 13 Iberian amphibian species, for instance, have their larval and embryo survival diminished due to predation by the red swamp crayfish. In addition, the alteration of water bodies’ conditions may also be a relevant factor (Cruz and Rebelo, 2005), once it has been proved that the macrophytes’ consumption by P. clarkii is directly associated to turbidity increase of the water (Rodríguez et al., 2003). Diamond (1996) reported egg, larval, and adult predation of the newt Taricha torosa by the red swamp crayfish, and it was also verified that P. clarkii is resistant to tetrodoxin, a bufadienolide toxin present in the newt’s skin and eggs’ membrane. This resistance may explain the fact that the crayfish can feed upon toads, such as Herpetology Notes, volume 6: 339-341 (2013) (published online on 23 August 2013) Predation of Rhinella ornata (Anura, Bufonidae) by the alien crayfish (Crustacea, Astacidae) Procambarus clarkii (Girard, 1852) in São Paulo, Brazil Karina R. S. Banci 1,2,* , Natália F. Torello Viera 1,2 , Patrícia S. Marinho¹, Pedro de O. Calixto 3 and Otavio A. V. Marques 1 1 Laboratório de Ecologia e Evolução, Instituto Butantan, CEP 05503-900, São Paulo Brazil. 2 Universidade Estadual Paulista (UNESP) – Campus de São José do Rio Preto – CEP 15054-000, São José do Rio Preto, Brazil. 3 STCP Engenharia de Projetos Ltda, CEP 80530-260, Curitiba, Brazil. *Corresponding author; e-mail: [email protected]

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Page 1: Predation of Rhinella ornata (Anura, Bufonidae) by the alien

The red swamp crayfish, Procambarus clarkii, is native from northern Mexico and south-central United States (Hobbs Jr., 1989). The species was introduced in several countries for aquaculture or to be used as a pet. Currently, its distribution comprises all the continents, except Australia and Antarctica (Huner, 1977). In Brazil the first report of its occurrence dates from the 1980’s, when the species could be found for sale in pet shops (Magalhães et al., 2005).

The introductions of the red crayfish on Latin America were motivated by the demand of United States’ market, where it is consumed (Hobbs III et al., 1989). In São Paulo State, southeastern Brazil, however, the species was most likely introduced to be used as pet, being dispersed throughout many water bodies in the region due to intentional or accidental release by aquarium keepers. Nowadays, P. clarkii can be found in the eastern São Paulo (Magalhães et al., 2005).

Rhinella ornata is a medium-sized frog that belongs to the family Bufonidae. It is a nocturnal and abundant species, found in open or forested areas in southeastern Brazil (Haddad et al., 2008). These toads are very well adapted to inhabit anthropized habitats (Baldissera, 2010).

On 15 August, 2012, during field work at night, two events of predation of R. ornata by P. clarkii were observed around 10:40 pm, in a swamp located at

Lymington Foundation (23.96478ºS 047.01452ºW), a reserve of Atlantic Forest, Juquitiba, São Paulo. One specimen of R. ornata was being attacked by four crayfishes, each of them clinging on a toad’s leg. When we approached, the toad and the crayfishes ran away. Another individual of this frog was being preyed by two crayfishes (Fig. 1). At this time, we captured the toad during the event of predation, and it showed lacerations on the abdomen and femoral musculature, as well as amputated feet (Fig. 2).

Reports on predation of R. ornata by invertebrates are already available in the literature, and, as seen now, it concurred with a reproductive explosion of the toads, when the males search actively for the females in water bodies (Haddad and Bastos, 1997).

Concerning the actual predator, P. clarkii, it has caused impact on the native fauna of several regions in the world, as shown in the following examples. This crustacean is the vector of the fungus Austrapotamobius pallipes, which causes the reduction of native crayfish species, such as the European crayfish Aphanomyces astaci (Gil-Sánchez and Alba-Tercedor, 2001). It has been already reported that P. clarkii may also cause high mortalities in amphibians (Cruz et al., 2006). The 13 Iberian amphibian species, for instance, have their larval and embryo survival diminished due to predation by the red swamp crayfish. In addition, the alteration of water bodies’ conditions may also be a relevant factor (Cruz and Rebelo, 2005), once it has been proved that the macrophytes’ consumption by P. clarkii is directly associated to turbidity increase of the water (Rodríguez et al., 2003).

Diamond (1996) reported egg, larval, and adult predation of the newt Taricha torosa by the red swamp crayfish, and it was also verified that P. clarkii is resistant to tetrodoxin, a bufadienolide toxin present in the newt’s skin and eggs’ membrane. This resistance may explain the fact that the crayfish can feed upon toads, such as

Herpetology Notes, volume 6: 339-341 (2013) (published online on 23 August 2013)

Predation of Rhinella ornata (Anura, Bufonidae) by the alien crayfish (Crustacea, Astacidae) Procambarus clarkii (Girard,

1852) in São Paulo, Brazil

Karina R. S. Banci1,2,*, Natália F. Torello Viera1,2, Patrícia S. Marinho¹, Pedro de O. Calixto3 and Otavio A. V. Marques1

1 Laboratório de Ecologia e Evolução, Instituto Butantan, CEP 05503-900, São Paulo Brazil.

2 Universidade Estadual Paulista (UNESP) – Campus de São José do Rio Preto – CEP 15054-000, São José do Rio Preto, Brazil.

3 STCP Engenharia de Projetos Ltda, CEP 80530-260, Curitiba, Brazil.

*Corresponding author; e-mail: [email protected]

Page 2: Predation of Rhinella ornata (Anura, Bufonidae) by the alien

Karina Rodrigues da Silva Banci et al.340

Figure 2. Injuries caused by Procambarus clarkii on a Rhinella ornata individual in Juquitiba, São Paulo, Brazil. Note the arrows evidencing the lacerations on the femur and abdomen, and fingers amputation.

Figure 1. Rhinella ornata being preyed by a crayfish in Juquitiba, São Paulo, Brazil.

Page 3: Predation of Rhinella ornata (Anura, Bufonidae) by the alien

Accepted by Philip de Pous

R. ornata, which also have bufadienolides in the skin (Akizawa et al., 1994).

The success of the P. clarkii in colonizing novel environments may be due to its rapid growth, high fecundity, polytrophy, aggressiveness, and resistance to toxins, diseases and adverse environmental conditions, being able to survive in shallow and ephemeral water bodies, burying during the dry seasons (Huner and Barr, 1984; Barbaresi and Gherardi, 2000). The place where predation occurred evidences this adaptation capacity to adverse conditions, once the water body was shallow and dirty.

Despite the fact that we did not estimate the predation rate during the events here reported, given the high plasticity of P. clarkii, and the increase on its distribution throughout the world, the already known impacts that it may cause to amphibian populations, it is crucial to conduct detailed studies concerning the real impacts caused by this crayfish on Brazilian amphibian populations. Such studies would provide subsidies for elaboration and implementation of conservation plans for the amphibians, and also strategies for population control of the crayfish. Considering that P. clarkii is a successful predator of a widespread and non threatened species such as R. ornata, it might form a severe threat to more endemic or threatened species. This threat becomes even more important considering that the crayfish is widespread among many water bodies in the Atlantic Forest, a biome that includes several endemic and threatened frog species (Haddad and Prado, 2008; Garcia et al., 2009).

Aknowledgements. We thank Célio F. B. Haddad for reviewing the manuscript, Bill and Linda from the Lymington Foundation, Cristiene R. Martins for editing the photos, and CNPq (INCTTox) and FAPESP for essential financial support.

References

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