35
OCCURRENCE OF TWO INDO-PACIFIC SPECIES OF BRACHYURA
ON THE COAST OF PIAUÍ, BRAZIL
Tarcísio Barbosa Lima Júnior 2
Mona I. da Costa Aragão1, 2
Janize Pereira da Silva1
Gustavo A. S. Melo3
José Roberto S. A. Leite1, 2
ABSTRACT
The occurrence of two species of Indo-Pacific origin, Pyromaia tuberculata (Lockington, 1877) and
Charybdis hellerii (A. Milne-Edwards, 1867) is reported from collections in areas of soft sediments in
the midlittoral zone in the coastal region of Luis Correia in the state of Piauí, which includes the Parnaíba
Delta Federal Environmental Protection Area. Both these species are presently well established in several
states of northeastern and southeastern Brazil.
Key-words: Brachyura, Exotic species, Parnaíba Delta, Piauí.
RESUMO
Ocorrência de duas espécies de Brachyura do Indo-Pacífico na Costa do Estado do Piauí,
Brasil
É relatada a ocorrência de duas espécies de origem Indo-Pacífica, Pyromaia tuberculata (Lockington,
1877) e Charybdis hellerii (A. Milne-Edwards, 1867), coletados em enclaves inconsolidados na zona de
mesolitoral da região costeira de Luis Correia, no Estado do Piauí, região que integra a Área de Proteção
Ambiental Federal Delta do Parnaíba. Atualmente estas espécies se encontram bem estabelecidas em
alguns Estados do Nordeste e Sudeste do Brasil.
Palavras-chave: Brachyura, Espécies Exóticas, Delta do Parnaíba, Piauí.
INTRODUCTION
Exotic, non-native or introduced species are
those that occur on a scale outside their historically
reported natural limit, as a result of accidental or
natural dispersal by human activities. They can also
occur by natural means, although generally on a
smaller spatial scale. In favorable conditions with
no predators, parasites or natural competitors, these
species can reach high population densities
(Carlton, 1987, 1989, 1996; Ruiz et al., 2000), and can
cause loss of biodiversity with the elimination of
native species, modify the trophic structure,
productivity and energy flow in ecosystems, and
generate economic impacts and health problems for
humans (Porter, 1999; Darrigran, 2002; Mansur et
al., 2003; Silva et al., 2004).
One of the most important mechanisms of
introduction of marine species into new areas by
humans is by shipping (Hutchings et al., 2002; Silva
et al., 2004). Ballast water is the principal dispersal
vector, and can transport, in addition to bacteria and
small invertebrates, eggs, cysts and larvae of larger
organisms. Because the great majority of marine
species have a life cycle with one or more planktonic
stages, even adults of species that live on hard
substrates or that are not pumped into ships because
of their larger size can be transferred to ballast-water
tanks in their larval forms and released in other ports,
when the ship is reloaded with freight (Carlton &
Geller, 1993). In consequence, thousands of marine
and estuarine species have been dispersed far from
their regions of origin (Vermeij, 1991; Ruiz et al., 1997;
Hutchings et al., 2002).
____________________________________________________________________________________________________________________________________________________________________________________________
1
Projeto Biodiversidade do Delta Conservação e Pesquisa - PROBID, Campus Ministro Reis Velloso, Universidade Federal
do Piauí - UFPI, Parnaíba, PI, 64202-020, Brazil; [email protected]
2
Instituto Ilha do Caju Ecodesenvolvimento e Pesquisa - ICEP, s/n, zona rural, Araioses, MA, 65570-000.
3
Museu de Zoologia da Universidade de São Paulo (MUZSP). Avenida Nazareth 481, Ipiranga, 04263-000, São Paulo, SP,
Brasil.
BOLETIM DO LABORATÓRIO DE HIDROBIOLOGIA, 21:35-40. 2008
36
LIMA-JÚNIOR et. al.
Transfer and introduction of these
organisms into new environments threaten the
conservation and sustainable use of biodiversity,
and is taken to be one of the four greatest threats to
marine environments (MMA, 2006). Often, even if
an introduced species has some ecological impact
on the environment or causes drastic changes in the
composition of the native communities, its advent
may occur without immediate detection, and once
the species is established, eradication is generally
difficult (Lodge, 1993; Carlton, 1996; Bax et al., 2001).
As a means of reducing the existing lacuna
in knowledge of the fauna of Brachyura in the state
of Piauí, the subproject "Carcinological
characterization of the coast of the State of Piauí"
("Caracterização carcinológica da costa do Estado
do Piauí)" was initiated in 2007 as part of the Delta
Biodiversity Project - Conservation and Research
(Projeto Biodiversidade do Delta - Conservação e
Pesquisa/PROBID). The principal objective of this
study was to record the exotic species of Brachyura
that occur on the coast of the Municipality of Luis
Correia in the state of Piauí, as an addition to the
inventory of marine biodiversity.
MATERIALAND METHODS
In august and september 2007, two species of
Brachyura of Indo-Pacific origin, Pyromaia
tuberculata (Lockington, 1877) and Charybdis
hellerii (A. Milne-Edwards, 1867), were collected
manually, in the midlittoral zone at low tide at the full,
on the beaches of Coqueiro (02°53'919"S :
41º33'515"W) and Macapá (02º54'815"S :
41°26'927"W), respectively. These beaches are located
on the coast of Luis Correia, Piauí, a region that
includes the Parnaíba Delta Environmental Protection
Area (Área de Proteção Ambiental Delta do Parnaíba
- APA) (Figure 1). Crabs were collected according to
the Instituto Brasileiro do Meio Ambiente e dos Recursos Renováveis, IBAMA, under the license
number 12529-1 SISBIO. The samples were
qualitative, with no standardized collecting effort.
The specimens were placed in test tubes and stored
frozen at -8°C to maintain their coloration. Later they
were fixed in 4% formol, conserved in 70% alcohol
and added to the carcinological collection of the
Paranaíba Delta Ecology Laboratory (Laboratório de
Ecologia Delta do Parnaíba - LEDP/UFPI/Parnaíba),
under numbers CCDP 0022 and CCDP 0034.
Figure 1. Localities of occurrence of the two exotic species on the
coast of the Municipality of Luis Correia, Piauí, Brazil.
BOLETIM DO LABORATÓRIO DE HIDROBIOLOGIA, 21:35-40. 2008
Occurrence of two Indo-Pacific species for the State of Piauí
37
RESULTS
Family Majidae
Pyromaia tuberculata (Lockington, 1877)
Figure 2. (A and B): Female of Pyromaia tuberculata (Lockington, 1877) (rostrum broken),
CCDP 0022: A -Dorsal view and B -Ventral view (Photo: Lima Júnior, T. B.).
Material examined: One ovigerous female: SL
6.5 mm and SW 4.9 mm, CCDP 0022. Diagnosis:
Carapace pyriform, flanks granulated and
tuberculate. One large tubercle, in some cases
spiniform, in the mesogastric, cardiac and intestinal
regions. First abdominal somite with short spiniform
tubercle. Rostrum simple (broken in the specimen
collected). One tubercle on supra-orbital surface of
carapace. Thoracic sternum granulate. Chelipeds
stout, with palm inflated, sparsely granulate. Female
smaller than male, more granulate, with smaller
median tubercles, rostrum shorter, abdomen
irregularly granulate, chelipeds more slender, palm
of cheliped only slightly inflated, fingers without
hiatus (after Melo, 1996).
Distribution: Species native to the Eastern
Pacific, from California, U.S.A., to Panama.
Introduced into Japan (Sakai, 1976), the western
Indo-Pacific (Grifffin & Tranter, 1986), Western
Australia (Morgan, 1990), and southeast Brazil,
where it is presently well established in the states of
Rio de Janeiro, São Paulo, Paraná and Rio Grande do
Sul (Melo et al., 1989; Melo, 1996; Tavares & Mendonça, 1996, 2004).
Family Portunidae
Charybdis hellerii (A. Milne-Edwards, 1867)
Material examined: SL, 41.6 mm; SW, 59 mm, CCDP 0034.
Figure 3. (A and B): Female of Charybdis hellerii (A. Milne-Edwards, 1867), CCDP 0034: A - Dorsal
view and B -Ventral view (Photo: Lima Júnior, T. B.).
BOLETIM DO LABORATÓRIO DE HIDROBIOLOGIA, 21:35-40. 2008
38
LIMA-JÚNIOR et. al.
Material examined: SL, 41.6 mm; SW, 59 mm,
CCDP 0034.
Diagnosis: Carapace with non-pilose dorsal
surface; antero-lateral margin with six acute teeth
(including the outer orbital). Frontal region with six
teeth: two inner orbital and four submedian. Chelae
strong; palm with five strong spines on dorsal
surface. Carpus and merus of natatory leg each armed
with one strong spine on distal part of posterior
margin; propodus with a row of spinules on posterior margin. Abdomen of male with sixth somite of
similar length and width, telson subtriangular. First
pleopod of male reaching approximately to suture
between fifth and sixth sternites (Coelho & Santos,
2003; Lemaitre, 1995; Carqueja & Gouvêa, 1996).
Distribution: Indo-Pacific: Japan, Philippines,
New Caledonia, Australia, Hawaii and the Indian
Ocean, including the Red Sea (Lemaitre, 1995);
Mediterranean Sea (Lemaitre, 1995); Western
Atlantic: Florida, Cuba, Colombia and Venezuela. In
Brazil the species was previously recorded in the
states of Rio Grande do Norte (Ferreira et al., 2001),
Pernambuco (Coelho & Santos, 2003), Alagoas (Calado, 1996), Bahia (Carqueija & Gouvêa, 1996), Rio
de Janeiro (Tavares & Mendonça, 1996), São Paulo
(Negreiros-Fransozo, 1996), Santa Catarina
(Mantelatto & Dias, 1999) and Ceará (Bezerra &
Almeida, 2005).
DISCUSSION
Of the eight species of marine decapods listed
as exotic by Tavares & Mendonça (1996), only two
species of Brachyura, Charybdis hellerii (A. MilneEdwards, 1867) and Pyromaia tuberculata
(Lockington, 1877), with very numerous populations
on the Brazilian coast, found relative success in their
introduction (Melo & Crivelaro, 2002). Recently, the
first occurrence in the Western Atlantic of Polybius
navigator (Herbst, 1794), a portunid of the Eastern
Atlantic and the Mediterranean Sea, was reported,
specifically in the state of Rio de Janeiro, Brazil.
However, all indications are that this species did not
have similar success in adapting to the Brazilian
coast, because it has been collected only once in
the past 35 years (Melo & Crivelaro, 2002).
In respect to Pyromaia tuberculata, there is
the possibility that reproducing populations are
establishing near Coqueiro Beach on the coast of
Luis Correia, because the material examined was an
ovigerous female. The species was collected within
areas of soft sediments in a region of rock outcrops.
The natural habitat of this species is algae-covered
rocky bottoms, and also under stones. It occurs from
the intertidal to 130 m, principally on soft muddy
bottoms (Melo, 1996). Populations of P. tuberculata
have established in Japan, in bays affected by
organic pollution and cycles of hypoxia, and it is
considered an opportunistic species. Studies in the
same country revealed that females reach maturity
within six months after settling, and also reach
maturity at a smaller size in high temperatures,
completing at least two reproductive cycles per year
(Furota, 1996 a, b). At the moment, it is not possible
to determine whether the introduction of this species
will negatively impact the study locale.
The portunid Charybdis hellerii, a "siri" with
no commercial value, is one of several known serious
cases, which is harming the fishery of the
corresponding native species in Bahia. There is a
risk that it will become a competitor of the
commercially important species and cause alterations
in the structure and taxonomic composition of their
populations (Tavares & Mendonça, 2004).
Charybdis hellerii was collected in the
estuarine system of Macapá Beach, where four
additional species of Portunidae were also recorded:
Callinectes danae Smith, 1869; Callinectes bocourti
(A. Milne-Edwards, 1879); Callinectes exasperatus
(Gerstaecker, 1856) and Callinectes larvatus Ordway,
1863. This highlights the importance of regular
surveys in the region, in order to analyze the impact
of this species on the environment and its
relationship with the native species.
The authors emphasized the necessity of
studying these introduced species, with emphasis
on gathering data on their abundance, reproductive
potential and relationship to the native species (Coelho & Santos, 2003). More extensive studies of the
systematics and biogeography are necessary in order
to determine more precisely the presence of nonnative organisms, as well as studies that envisage
developing means for the control of their populations
in Brazil. There are few control methods for these
species in Brazilian waters (Neves, 2006). The paucity
of studies on faunal surveys, biogeographical tanges, and adequate monitoring impede the detection
of non-native species in a given locale.
The chances of eradication of these species
in the study areas may be small, although their
populations can be studied and thus monitored. The
information provided here can contribute to future
assessments of the biodiversity of this region,
besides supporting the development of plans for
the management and conservation of the areas
studied, and contributing necessary information to
BOLETIM DO LABORATÓRIO DE HIDROBIOLOGIA, 21:35-40. 2008
Occurrence of two Indo-Pacific species for the State of Piauí
improve knowledge of the exotic species that occur
in the Parnaíba Delta Environmental Protection Area.
Acknowledgments
The authors thank the Projeto Biodiversidade
do Delta - Conservação e Pesquisa (PROBID), Instituto Ilha do Caju Ecodesenvolvimento e Pesquisa
(ICEP), Projeto Cetáceos Maranhão (PROCEMA),
Universidade Federal do Piauí, and Petrobrás
Ambiental Programe for logistical and financial
support. We also thank Wennys Dean Sousa da Silva (Universidade Federal do Piauí) for developing
the maps of the occurrences of the species treated
herein.
REFERENCES
BAX, N., CARLTON, J.T., MATHEWS-AMOS, A.,
HAEDRICH, R.L., HOWARTH, F.G., PURCELL, J.E.,
RIESE, A. & GRAY, A. 2001. The control of biological
invasion in the world's ocean. Conservation Biology,
15 (5): 1234 - 1246.
BEZERRA, L.E.A. & ALMEIDA, A.O. 2005. Primeiro
registro da espécie Indo-Pacífica Charybdis hellerii
(A. Milne - Edwards, 1867) (Crustacea: Decapoda:
Portunidae) para o litoral do Estado do Ceará. Tropical Oceanography, 33(1): 33-38.
CALADO, T.C.S. 1996. Registro de Charybdis
hellerii (Milne Edwards, 1867) em águas do litoral
brasileiro (Decapoda: Portunidae). Bol. Est. Ciên.
Mar, Maceió, 9: 175-180.
CARLTON, J.T. 1987. Patterns of transoceanic marine
biological invasions in the Pacific Ocean. Bulletin
of Marine Science, 41 (2): 452 - 465.
CARLTON, J.T. 1989. Man´s role in changing the
face of the ocean: biological invasions and
implications for conservation of near-shore
environments. Conservation Biology, 3 (3): 265-273.
CARLTON, J.T. 1996. Pattern, processes and
prediction in marine invasion ecology. Biological
Conservation, 7: 97-106.
CARLTON, J.T. & GELLER, J.B. 1993. Ecological
roulette: the global transport of nonindigenous
marine organisms. Science, 261: 78-82.
CARQUEIJA, C.R.G. & GOUVÊA, E.P. 1996. A ocorrência, na costa brasileira, de um Portunidae
(Crustacea: Decapoda), originário do Indo-Pacífico
e Mediterrâneo. Nauplius, 4: 105-112.
39
COELHO, P.A. & SANTOS, M.C.F. 2003. Ocorrência
de Charybdis hellerii (Milne Edwards, 1867)
(Crustacea, Decapoda, Brachyura) no Litoral de
Pernambuco. Boletim Técnico Científico CEPENE,
11 (1): 167-173.
DARRIGRAN, G. 2002. Potential impact of filterfeeding invaders on temperate inland freshwater
environments. Biological Invasions, 4:145-156.
FERREIRA, A.C., SANKARANKUTY, C., CUNHA,
I.M.C. & DUARTE, F.T. 2001. Yet another record of
Charybdis hellerii (A. Milne-Edwards) (Crustacea,
Decapoda) from the Northeast of Brazil. Revista Brasileira de Zoologia, 18 (supl. 1): 357-358.
FUROTA, T. 1996a. Life cycle studies on the
introduced spider crab Pyromaia tuberculata
(Lockington) (Brachyura: Majidae). I: Egg and larval
stages. Journal of Crustacean Biology, 16: 71-76.
FUROTA, T. 1996b. Life cycle studies on the
introduced spider crab Pyromaia tuberculata
(Lockington) (Brachyura: Majidae). II: Crab stage
and reproduction. Journal of Crustacean Biology,
16: 77-91.
GRIFFIN, D.J.G. & TRANTER, H.A. 1986. The
Decapoda Brachyura of the Siboga Expedition. Part
VIII. Majidae. In: Siboga-Expeditie Monographie,
39: 1-335. E. J. Brill, Leiden.
HUTCHINGS, P.A., HILLIARD, R. W. & COLES, S.L.
2002. Species introductions and potential for marine
pest invasions into tropical marine communities, with
special reference to the Indo-Pacific. Pacific Science,
56 (2): 223-233.
LEMAITRE, R. 1995.Charybdis hellerii (Milne
Edwards, 1867), a nonindigenous portunid crab
(Crustacea, Decapoda, Brachyura), discovered in the
Indian River lagoon system of Florida. Proceedings
of the Biological Society of Washington, 108 (4):
643-648.
LODGE, D.M. 1993. Biological invasions: lessons of
ecology. Trends in Ecology and Evolution, 8: 133136.
MANSUR, M.C., SANTOS, C.P., DARRIGRAN, G.,
HEYDRICH, I., CALLIL, C.T. & CARDOSO, F.R. 2003.
Primeiros dados quali-quantitativos do "mexilhão
dourado", Limnoperna fortunei (Dunker, 1857), no
lago Guaíba, Bacia da laguna dos Patos, Rio Grande
do Sul, Brasil e alguns aspectos de sua invasão no
novo ambiente. Revista Brasileira de Zoologia, 22
(1): 75-84.
BOLETIM DO LABORATÓRIO DE HIDROBIOLOGIA, 21:35-40. 2008
40
LIMA-JÚNIOR et. al.
MANTELATTO, F.L.M. & DIAS, L.L. 1999. Extension
of the known distribution of Charybdis hellerii (A.
Milne-Edwards, 1867) (Decapoda, Portunidae) along
the western tropical South Atlantic. Crustaceana,
72 (6): 617-620.
MELO, G.A.S. 1996. Manual de identificação dos
Brachyura (caranguejos e siris) do litoral brasileiro. São Paulo, Editora Plêiade/ Fapesp, 603p.
MELO, G.A.S. & CRIVELARO, T.B. 2002. Primeira
ocorrência de Polybius navigator (Herbst)
(Decapoda, Brachyura, Portunidae) no Atlântico
Ocidental. Revista Brasileira de Zoologia, 19 (1):
233-238.
MELO, G.A.S., VELOSO, V.G. & OLIVEIRA, M.C.
1989. A fauna de Brachyura (Crustacea, Decapoda)
do litoral do estado do Paraná. Lista preliminar, Pontal
do Sul - PR, 4. Neritica, 4 :1-31.
MINISTÉRIO DO MEIO AMBIENTE, MMA. 2006.
Available at: <http://www.mma. gov.br/port/sqa/
projeto/lastro/problem.html> accessed on 19
October 2007.
MORGAN, G.J. 1990. An introduced Eastern Pacific
majid crab from Cockburn Sound, Southwestern
Australia. Crustaceana, 58: 316- 317.
NEGREIROS-FRANZOSO, M.L. 1996. The zoea I of
Charybdis hellerii (A. Milne-Edwards, 1867)
(Decapoda, Portunidae) obtained in laboratory.
Nauplius, 4: 165-168.
NEVES, C.S. 2006. Bioinvasão mediada por embarcações de recreio na Baía de Paranaguá, PR e suas
implicações para a conservação. Pós-graduação em
Ecologia e Conservação, Setor de Ciências Biológicas da Universidade Federal do Paraná.
PORTER, M. de, 1999. Borrador de Guías para la
prevención de pérdidas de diversidad biológica ocasionadas por invasion biológica. Cuarta Reunión del
Órgano Subsidiario de Asesoramiento Científico, Técnico y Tecnológico. Documento de Base. Unión Internacional para la Naturaleza. 15 p.
RUIZ, G.M., CARLTON, J.T., GROSHOLZ, E.D., &
HINES, A.H. 1997. Global invasion of marine and
estuarine habitats by non-indigenous species:
mechanisms, extent and consequences. American
Zoologist, 37: 621-632.
RUIZ, G. M.; FOFONOFF, P. W.; CARLTON, J. T.;
WONHAN, M. J. & HINES, A. H. 2000. Invasion of
coastal marine communities in North America:
apparent patterns, processes and biases. Annual
Review of Ecological Systems, 31: 481-531.
SAKAI, T. 1976. Crabs of Japan and the Adjacent
Seas. Tokio, Kodansha, 773 pp.
SILVA, J. S. V.; DA COSTA, F.; CORREA, R. C.;
SAMPAIO, K. T. & DANELON, O. M. 2004. Água de
lastro e bioinvasão. p. 1-10 In: Silva & Souza (eds)
Água de lastro e bioinvasão. Rio de Janeiro.
Interciência.
TAVARES, M. & MENDONÇA JR., J.B. 1996.
Charybdis hellerii (A. Milne Edwards, 1867)
(Brachyura: Portunidae), eighth nonindigenous marine
decapod from Brazil. Crustacean Researches, 25: 151157.
TAVARES, M. & MENDONÇA JR., J.B. 2004. Introdução de crustáceos decápodes exóticos no Brasil. p.
59-76 In: Silva, J. S. V. and Souza, R. C. C. L. de (orgs.)
Água de lastro e bioinvasão. Rio de Janeiro:
Interciência.
VERMEIJ, G.J. 1991. When biotas meet: understanding
biotic interchange. Science, 253 (5024): 1099-1104.
Recebido em 5 de maio de 2008.
Aprovado em 16 de junho de 2008.
BOLETIM DO LABORATÓRIO DE HIDROBIOLOGIA, 21:35-40. 2008