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Predation of Rhinella ornata (Anura, Bufonidae) by the alien crayfish (Crustacea, Astacidae) Procambarus clarkii (Girard, 1852) in São Paulo, Brazil

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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)
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The red swamp craysh, 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 rst 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 craysh 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 eld 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
crayshes, each of them clinging on a toad’s leg. When
we approached, the toad and the crayshes ran away.
Another individual of this frog was being preyed by two
crayshes (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 craysh
species, such as the European craysh 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 craysh. 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
craysh, and it was also veried 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 craysh 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
craysh (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: karina.banci@gmail.com
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 ngers amputation.
Figure 1. Rhinella ornata being preyed by a craysh in Juquitiba, São Paulo, Brazil.
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 craysh 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 craysh. 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
craysh 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 nancial support.
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Predation of Rhinella ornata (Anura, Bufonidae) by the alien craysh 341
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Les auteurs donnent un aperçu de l'introduction d'écrevisses exotiques à travers le monde depuis 1746. Les transplantations constatées par des documents ont une très large extension géographique et beaucoup d'autres n'ont sans doute jamais été signalées. Deux espèces d'origine nord-américaine ont été introduites avec un succès particulier: ce sont Orconectes rusticus, qui a été implanté en diverses régions des Etats-Unis et Procambarus clarkii, qui l'a été sur tous les continents, Antarctique et Australie exceptés. Dans la plupart des cas, quand ces espèces ont été établies, elles ont entraîné des changements drastiques dans la structure des communautés, avec le remplacement ou la réduction des populations d'écrevisses indigènes. Beaucoup de recherches sont nécessaires pour comprendre les mécanismes de remplacement des espèces (par exemple, exclusion compétitive, recrutement et croissance différentiels, subordination agressive) et leurs implications à long terme en ce qui concerne la structure des écosystèmes aquatiques. Les écrevisses exotiques fournissent certes de la nourriture pour l'Homme, mais les effets négatifs sont considérables et les transplantations extensives sont à décourager.
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The introduction of predators in amphibian breeding habitats may contribute to the decline or extinction of amphibian populations. Procambarus clarkii, a North American crayfish, was recently introduced in the Iberian Peninsula, being now quite abundant in the southwest, a region with no native crayfish species and where 13 amphibian species may be found. We performed mesocosm experiments to evaluate the vulnerability of amphibian embryos and larvae from those species to P. clarkii. Despite the presence of alternative food (vegetation and leaf litter), embryo survival in the presence of P. clarkii was low for all species except Bufo bufo. However, newly hatched B. bufo tadpoles were readily consumed. P. clarkii reduced larval survival in all species, with those species that in nature have few contacts with predators at the larval stage suffering the highest mortalities. Most larvae reduced their activity and/or altered microhabitat use in the presence of P. clarkii, but these behavioural modifications did not lead necessarily to a low vulnerability to predation.
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Over the last two decades, numerous studies have shown that alien predators contributed to amphibian population declines. Both experimental studies and correlative field surveys implicated alien species of fish, bullfrogs and crayfish as major contributors to amphibian population decline, and in some instances local extinction. Additional studies have demonstrated that alien predators also caused long-term changes in aquatic communities. Recent studies have examined the feasibility of removing alien predators, and provide some evidence that amphibian populations can recover. Applying information gained from past studies to the recovery of amphibian populations will be the challenge of future studies. International, national and local policies that regulate alien predators should be based largely on the body of scientific evidence already in the literature. Scientists need to be more involved with policy-makers to most effectively change laws that regulate alien predators.
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The introduction of exotic species in aquatic habitats is one of the causes for the amphibian declines observed worldwide. In the 1970s, the red swamp crayfish Procambarus clarkii was introduced in the southwest Iberian Peninsula, where no native crayfish occur. In this study we assess the effect of P. clarkii presence in the breeding site distribution of each of the 13 southwest Iberian amphibians, while simultaneously accounting for the effects of potentially confounding habitat variables, as well as for the effects of the other large aquatic predators in the study area – predatory fish. Amphibian species richness was lower in places where P. clarkii was present than in places without P. clarkii, regardless of fish presence. After accounting for habitat variables and fish, crayfish presence was a negative predictor of the breeding probability for all urodeles (Pleurodeles waltl, Salamandra salamandra, Triturus boscai and T. marmoratus) and for two anurans (Pelobates cultripes and Bufo bufo). The majority of the species affected usually breed in temporary ponds without fish, but that may be colonized by the crayfish. The ongoing expansion of P. clarkii may eventually lead to a growing isolation of amphibian populations and ultimately to local extinctions and a permanent alteration of the amphibian communities in southwest Iberian Peninsula.