Predation of Rhinella ornata

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
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
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]
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
340
Karina Rodrigues da Silva Banci et al.
Figure 1. Rhinella ornata being preyed by a crayfish in Juquitiba, São Paulo, Brazil.
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.
Predation of Rhinella ornata (Anura, Bufonidae) by the alien crayfish
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
Akizawa, T., Mukai, T., Matsukawa, M., Yoshioka, M., Morris,
J.F., Butler, V.P. (1994): Structures of novel bufadienolides in
the eggs of a toad, Bufo marinus. Chemical and Pharmaceutical
Bulletin 42: 754-756.
Baldissera, F. (2010): Rhinella ornata. IUCN Red List of
Threatened Species, Version 2012.2. Available at: http://www.
iucnredlist.org. Last accessed on 31 January 2013.
Barbaresi, S., Gherardi, F. (2000): The invasion of the alien
crayfish Procambarus clarkii in Europe, with particular
reference to Italy. Biological Invasions 2: 259-264.
Correia, A.M. (2003): Food choice by the intorduced crayfish
Procambarus clarkii. Annales Zoologici Fennici 40: 517-528.
Cruz, M.J., Rebelo, R. (2005): Vulnerability of Southwest Iberian
amphibians to an introduced crayfish, Procambarus clarkii.
Amphibia-Reptilia 26: 293-303.
341
Cruz, M.J., Rebelo, R, Crespo, E.G. (2006): Effects of an
introduced crayfish, Procambarus clarkii, on the distribution
of south-western Iberian amphibians in their breeding habitats.
Ecography 29: 329-338.
Diamond, J.M. (1996): A-bombs against amphibians. Nature 383:
386-387.
Garcia, P.C.A.; Sawaya, R.J.; Martins, I.A.; Brasileiro, C.A.;
Verdade, V.K.; Jim, J.; Segalla, M.V.; Martins, M.; RossaFeres, D.C.; Haddad, C.F.B.; Toledo, L.F.; Prado, C.P.A.;
Berneck, B.M.; Araújo, O.G.S. (2009): Anfíbios. In: Fauna
Ameaçada de Extinção do Estado de São Paulo: Vertebrados,
p. 329-347. Bessan, P.M.; Kierulff, M.C.M.; Sugieda, A.M.,
Ed., São Paulo, Fundação Parque Zoológico de São Paulo,
Secretaria do Meio Ambiente.
Gil-Sánchez, J.M., Alba-Tercedor, J. (2002): Ecology of the
native and introduced crayfishes Austrapotamobius pallipes
and Procambarus clarkii in southern Spain and implications
for conservation of the native species. Biological Conservation
105: 75-80.
Haddad, C.F.B.; Bastos, R.P. (1997): Predation on the toad Bufo
crucifer reproduction (Anura: Bufonidae). Amphibia-Reptilia
18: 295-298.
Haddad, C.F.B.; Prado, C.P.A. (2005): Reproductive modes on
frogs and their unexpected diversity in the Atlantic Forest of
Brazil. Bioscience 55: 207-217.
Haddad, C.F.B.; Toledo, L.F. & Prado, C.P.A. (2008): Anfíbios da
Mata Atlântica. 1st Edition. São Paulo, Editora Neotropica.
Hobbs III, H.H., Jass, J.P., Huner, J.V. (1989): A review of global
crayfish introductions with particular emphasis on two North
American species (Decapoda, Cambaridae). Crustaceana 56:
299-316.
Hobbs, Jr., H.H. (1989): An illustrated checklist of the
American crayfishes (Decapoda: Astacidae, Cambaridae, and
Parastacidae). 1st Edition. Washington, D.C., Smithsonian
Institution Press.
Huner, J.V. (1977): Introductions of the Louisiana red swamp
crayfish, Procambarus clarkii (Girard): an update. Freshwater
Crayfish 3: 193-202.
Huner, J.V., Barr, J.E. (1984): Red swamp crayfish: biology and
exploitation (revised). Louisiana, Louisiana Sea Grant College
Program, Center for Wetland Resources.
Huner, J. V., Avault, Jr., J. W. (1979): Introductions of Procambarus
spp. Freshwater Crayfish 4: 191-194.
Kats, L.B., Ferrer, R.P. (2003): Alien predators and amphibian
declines: review of two decades of science and the transition to
conservation. Diversity and Distributions 9: 99-110.
Magalhães, C., Bueno, S.L.S., Bond-Buckup, G., Valenti, W.C.,
Silva, H.L.M., Kiyohara, F., Mossolin, E.C., Rocha, S.S.
(2005): Exotic species of freshwater decapods crustaceans in
the state of São Paulo, Brazil: records and possible causes of
their introduction. Biodiversity and Conservation 14: 19291945.
Rodríguez, C.F., Bécares, E., Fernández-Aláez, M. (2003): Shift
from clear to turbid phase in Lake Chozas (NW Spain) due to
the introduction of American red swamp crayfish (Procambarus
clarkii). Hydrobiologia 506-509: 421-426.
Accepted by Philip de Pous