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Exotic species of freshwater decapod crustaceans in
the state of Sa
˜o Paulo, Brazil: records and possible
causes of their introduction
CE
´LIO MAGALHA
˜ES
1,6,*
,SE
´RGIO LUIZ S. BUENO
2
,
GEORGINA BOND-BUCKUP
3,6
, WAGNER COTRONI VALENTI
4,6
,
HUMBERTO L. MELO DA SILVA
5
,FA
´BIO KIYOHARA
5
,
EMERSON C. MOSSOLIN
5
and SE
´RGIO S. ROCHA
5
1
Instituto Nacional de Pesquisas da Amazo
ˆnia, Caixa Postal 478, 69011-970 Manaus, AM, Brazil;
2
Departamento de Zoologia, Instituto de Biocie
ˆncias, Universidade de Sa
˜o Paulo, Sa
˜o Paulo, SP,
Brazil;
3
Departamento de Zoologia, Instituto de Biocie
ˆncias, Universidade Federal do Rio Grande do
Sul, Porto Alegre, RS, Brazil;
4
Departamento de Biologia Aplicada, Universidade Estadual Paulista,
Jaboticabal, SP, Brazil;
5
Curso de Po
´s-Graduac¸a
˜o em Zoologia, Instituto de Biocie
ˆncias, Univer-
sidade de Sa
˜o Paulo, Sa
˜o Paulo, SP, Brazil;
6
Research Fellow of the Conselho Nacional de
Desenvolvimento Cientı´fico e Tecnolo
´gico (CNPq); *Author for correspondence (e-mail: celiomag@
inpa.gov.br)
Received 4 July 2003; accepted in revised form 23 February 2004
Key words: Anthropogenic dispersal, Biological invasion, Brazil, Crustacea, Decapoda, Exotic
species, Freshwater, Sa
˜o Paulo
Abstract. Based on recent surveys of the freshwater decapod fauna, distributional data of five
exotic species of freshwater decapod crustaceans for the hydrographic basins of the state of Sa
˜o
Paulo are presented, as part of a large initiative for a comprehensive survey of the state’s biodi-
versity (BIOTA-FAPESP Program). These species are the North American crayfish Procambarus
clarkii (Girard) (Cambaridae), the crab Dilocarcinus pagei Stimpson (Trichodactylidae) from the
Amazon and Paraguay/lower Parana
´River Basins, and the palaemonid shrimps Macrobrachium
rosenbergii (De Man), from the Indo-Pacific region, Macrobrachium amazonicum (Heller) and
Macrobrachium jelskii (Miers), both from the Orinoco, Amazon and the Paraguay/lower Parana
´
River Basins. Possible modes by which their introduction might have occurred are commented
upon and potential consequences are discussed.
Introduction
Introduction of decapod crustaceans in regions other than their natural dis-
tribution areas has been mentioned several times in scientific literature. Rod-
rı
´guez and Sua
´rez (2001) summarized many documented cases of
anthropogenic dispersal of marine and freshwater decapod species, and dis-
cussed possible factors that could account for their dispersal. Although there
are some well known cases of introduction of marine decapod species in Brazil,
(Melo 1983, 1989; Bueno 1989; Barreto et al. 1991/1993; Calado 1996; Car-
queija and Gouveˆ ia 1996; Negreiros-Fransozo 1996; Tavares and Mendonc¸ a
1996; Mantelatto and Dias 1999; Melo et al. 2000; Severino-Rodrigues et al.
2000; Mantelatto and Garcia 2001; Melo and Crivelaro 2002), information on
Biodiversity and Conservation (2005) 14: 1929–1945 Springer 2005
DOI 10.1007/s10531-004-2123-8
the dispersal of freshwater shrimps and crabs due to human activities is sparse
or poorly documented, with few notable exceptions such as reports of the Indo-
Pacific shrimp, Macrobrachium rosenbergii (De Man) in the natural environ-
ment of the eastern Amazon region (Barros and Silva 1997; Valenti and New
2000) and in the state of Espı
´rito Santo (Valenti and New 2000).
The freshwater decapod fauna in the state of Sa
˜o Paulo is relatively well
known. The first well established records were made by Ortmann (1897) and
H. von Ihering (1897). Subsequent authors enhanced this knowledge either by
recording additional species or by describing new ones (see Magalha
˜es 1999a for
a review of the literature). Magalha
˜es (1999a) summarized the knowledge on the
diversity of freshwater decapods in the state of Sa
˜o Paulo by listing 32 species
from five families and eight genera. He mentioned the presence of some exotic
species but did not make further comments about their occurrence in Sa
˜o Paulo.
In fact, data concerning the occurrence of exotic freshwater decapods in Sa
˜o
Paulo are sporadic and mostly available as meeting abstracts only (see, for in-
stance, Hirose et al. 2000; Silva et al. 2000; Suzuki et al. 2000; Bueno et al. 2001).
Recent collections for inventorying the freshwater decapod fauna, conducted
as part of the BIOTA-FAPESP Program, a large initiative for a comprehensive
survey of the state’s biodiversity, produced more consistent distributional data
on this fauna. In the present paper, we discuss the occurrence of five exotic
decapod crustaceans in the state of Sa
˜o Paulo, and comment possible modes by
which their introduction might have occurred as well as potential consequences.
Materials and methods
Data on the occurrence of the species were obtained from field collections
conducted by the authors, from specimens in scientific collections, from pub-
lished or unpublished literature (congress abstracts, technical reports), and from
personal observation. The specimens were deposited in the collections of the
Museu de Zoologia (MZUSP) and Departamento de Zoologia, Instituto de
Biocieˆ ncias (DZ-USP), Universidade de Sa
˜o Paulo, Sa
˜o Paulo; Departamento
de Zoologia, Universidade Federal do Rio Grande do Sul, Porto Alegre
(UFRGS); and Instituto Nacional de Pesquisas da Amazoˆ nia, Manaus (INPA).
Other abbreviations are: juv. = juveniles; ov. = ovigerous; RPPN = Reserva
Privada do Patrimoˆ nio Natural; spec. = specimens. Terms related to species
introductions follow the definitions used by Holdich and Gherardi (1999).
Results
Cambaridae Hobbs Jr.
Procambarus clarkii (Girard)
Material – Brazil, Sa
˜o Paulo: Taubate
´,co
´rrego no bairro Vila Nogueira,
2300¢48¢¢S4533¢31¢¢N, 9.xii.2003, 1#(MZUSP 16124); Rio Tieteˆ Basin, Sa
˜o
1930
Paulo, Parque Municipal Alfredo Volpi, 2335¢16¢¢S4642¢09¢¢W, 22.vii.1999,
2$(MZUSP 14501); idem, 14.ix.1999, 2 spec. (MZUSP 14502); idem,
17.ix.1999, 3 spec. (MZUSP 14503); idem, 15.x.1999, 3#1$3 juv. (MZUSP
14504); idem, 29 spec. (MZUSP 14505); idem, 10.xii.1999, 16 spec. (MZUSP
14506); idem, 21.xii.1999, 8 spec. (MZUSP 14507); idem, 27.vii.2000, 1 ov. $
(MZUSP 14508); idem, 29.xi.2000, 1 ov. $(MZUSP 14509); idem, 20.ii.2001, 1
ov. $(MZUSP 14510); idem, 15.iii.2001, 1 ov. $(MZUSP 14511); idem, 4#5$
(INPA 871); idem, 4#,2$, 24.xii.1990 (UFRGS 03102); Sa
˜o Paulo, bairro do
Butantan, iii.1996, 1#(MZUSP 11271); Rio Tieteˆ Basin, Embu, bairro de
Itatuba, pesqueiro do Gau´ cho, 2338¢07,9¢¢S4653¢45,1¢¢W, 5.ii.2002, 8#3$
(MZUSP 15001); idem, 6#5$(MZUSP 15002); idem, 4.ii.2002, 2 spec.
(MZUSP 15003); idem, 3 spec. (MZUSP 15004); Rio Tieteˆ Basin, Embu,
co
´rrego do bairro de Itatuba, 2337¢55,3¢¢S4653¢35,4¢¢W, 4.ii.2002, 6#6$
(MZUSP 15005).
Remarks – The crayfish Procambarus clarkii is native to south-central
United States and northeastern Mexico, and has a distributional range
extending from northern Mexico to Florida, southern Illinois and Ohio, in the
United States (Hobbs Jr. 1989). Due to its commercial significance both in
terms of fisheries and aquaculture or as an aquarium animal, the species has
successfully been introduced in several countries around the world (Huner
1977, 1986, 1995; Hobbs III et al. 1989; Henttonen and Huner 1999; Rodrı
´guez
and Sua
´rez 2001). In Brazil, the first report of its occurrence was provided by
Huner (1986) based on an account made to him about a successful introduction
around the city of Sa
˜o Paulo (J. Huner, in litt. to C.M.). We observed the
commercial selling of this species in some pet shops back in 1985 and it con-
tinues as strong as ever today. So far the only confirmed records of a natural
environment colonization by P. clarkii in Brazil are the ones made above.
Palaemonidae Rafinesque
Macrobrachium rosenbergii (De Man)
Material – Brazil, Sa
˜o Paulo: Rio Tieteˆ Basin, Brejo Alegre, 2107¢S5010¢W,
i.2001, 1#(MZUSP 13918); Pindamonhangaba, viveiros experimentais de
cultivo do Instituto de Pesca, no date and collector, 1#(MZUSP 13456); idem,
1#(MZUSP 13457); idem, 1#(MZUSP 13458); criac¸ a
˜o, Instituto de Pesca,
1988, 1 ov. $(MZUSP 9588); idem, 1#(MZUSP 9589); cultivado no Instituto
de Pesca, 1985, 1#(MZUSP 7170); several juv. (UFRGS 756); idem (UFRGS
815); 3#,1$(UFRGS 816), from Instituto de Pesca – SP, 19.iii.985; 1#
(UFRGS 882), Sa
˜o Paulo, 3.iii.1985; 1#(UFRGS 00883), Sa
˜o Paulo, 3.iii.1985.
Remarks – The species is characterized by the long rostrum bearing 11–14
dorsal and 8–10 ventral teeth, with the tip slightly curved upwards. Telson has
a distinct posterior margin, with the median point not overreached by the inner
pair of posterior spines. Adult males have very long, strong second pereiopods,
usually with blue or orange color. Although morphologically similar to
1931
M. amazonicum, the asiatic species has more teeth in the dorsal margin of the
rostrum, which are more regularly spaced in its distal portion, and its chelipeds
are clearly stronger then those of M. amazonicum. In addition, M. rosenbergii
reaches a very large size with a very robust appearance. Except for the large
male specimen from Brejo Alegre (Rio Tieteˆ Basin) that was actually caught in
the wild, all other M. rosenbergii listed herein are from freshwater shrimp
culture facilities.
Macrobrachium amazonicum (Heller)-Figure 1(1, 2)
Material – Brazil, Sa
˜o Paulo: branch of Rio Grande, between Mira Estrela and
Cardoso, 2001¢51¢¢S5000¢59¢¢W, 23.i.2003, 6$(1 ov.) (MZUSP 15794); Rio
Turvo, between Riolaˆ ndia and Cardoso, 2004¢29¢¢S4948¢46¢¢W, 23.i.2003, 3$
(1 ov.), (MZUSP 15598); 5 km S of Santa Fe
´do Sul, between Santa Fe
´do Sul
and Canaa
˜,2017¢35¢¢S5055¢17¢¢W, 22.i.2003, 9$(2 ov.) (MZUSP 15576);
Jupia
´,2045¢54¢¢S5135¢32¢¢W, 22.i.2003, 3#1$(15580); Buritama, 2105¢55¢¢S
5010¢31¢¢W, 1#4$(1 ov.) (15600); Rio Tieteˆ , reservato
´rio de Treˆ s Irma
˜os,
ii.2000–vi.2000, 54 spec. (8 ov. $) (MZUSP 13465); Rio Tieteˆ Basin, Pena
´polis,
Figure 1. (1–5) Macrobrachium amazonicum (Heller), adult #, INPA 873. (1) Anterior part of
carapace and rostrum, lateral view. (2) telson, dorsal view. Macrobrachium jelskii (Miers), adult #,
INPA 585; (3) anterior part of carapace and rostrum, lateral view (4) telson, dorsal view. Dilo-
carcinus pagei Stimpson, #, INPA 872; (5) distal part of the first gonopod, mesio-ventral view.
1932
18.xi.2001, 29 spec. (5 ov. $) (INPA 886); Rio Parana
´, Reserva Florestal Lagoa
Sa
˜o Paulo, Campinal, 2131¢35¢¢S5200¢33¢¢W, 15.x.2002, 12#10$(MZUSP
15573); Rio Tieteˆ Basin, Lins, RPPN Dr. Ivan, 2134¢18¢¢S4938¢19¢¢W,
21.i.2003, 2#7$(2 ov.) (MZUSP 15608); Rio Parana
´,Co
´rrego Veado, Presi-
dente Epita
´cio, 2143¢16¢¢S5202¢11¢¢W, 15.x.2002, 14#21$(MZUSP 15603);
Rio do Peixe, Flora Rica, between Flora Rica and Santo Expedito, 2144¢19¢¢S
5122¢45¢¢W, 16.x.2002, 1#1$(MZUSP 15596); Rio Parana
´, Ribeira
˜o Cai-
uazinho, Presidente Epita
´cio, 2145¢39¢¢S5245¢07¢¢W, 15.x.2002, 19#13$
(MZUSP 15574); Rio do Peixe, between Parapua
˜and Martino
´polis,
2156¢56¢¢S5056¢23¢¢W, 16.x.2002, 2#(MZUSP 15602); dam at rio Cascata,
Rio do Peixe Basin, Marı
´lia, 2212¢50¢¢S4955¢29¢¢W, 18.x.2002, 11#4$
(MZUSP 15572); Rio Parana
´, Primavera, 2231¢03¢¢S5259¢47¢¢W, 14.x.2002,
15#16$(MZUSP 15601); Rio Paranapanema Basin, Sandovalina,
2233¢75.0¢¢S5154¢61.5¢¢W, 24.viii.2000, 1 spec. (MZUSP 13917); Sandovali-
na, rio Paranapanema, 2233¢78.0¢¢S5154¢69.3¢¢W, 24.viii.2000, 23 spec.
(MZUSP 13916); idem, 10 spec. (INPA 873); Rosana, Rosana hydroeletric
dam, 2236¢32¢¢S5251¢45¢¢S, 14.x.2002, 9#19$(MZUSP 15589); Sandovalina,
2239¢26.8¢¢S5125¢11.2¢¢W, 25.viii.2000, 25 spec. (DZ-USP); Rio Paranapa-
nema, Salto Grande hydroeletric dam, Salto Grande, 2254¢07¢¢S5000¢02¢¢W,
12.x.2002, 9#35$(MZUSP 15607); Rio Paranapanema, Chavantes hydro-
eletric dam, Chavantes, 2306¢37¢¢S4943¢25¢¢W, 11.x.2002, 13#17$(MZUSP
15577); Rio Paranapanema Basin, Piraju´ ,2311¢06¢¢S4922¢43¢¢W, 10.x.2002,
1#(MZUSP 15582).
Remarks – Adults of M. amazonicum are easily characterized by the long
and sinuous rostrum, which is arched over the orbits and obliquely curved
upwards in its distal portion, and by the conical shape of the telson, which
tapers gradually towards the tip. The posterior margin ends in an acute median
point with no distinct discontinuity and bears two pairs of spines, the inner one
not overreaching the apex of the telson. However such characters are not so
marked in juveniles and immature specimens, which add some difficulties to
their identification. At this stage, they could be confused with M. jelskii or even
M. acanthurus, which have similar morphology. Ovigerous females of
M. amazonicum carry numerous and relatively small eggs, from which a zoea
larva hatches; its larval development can present as many as 11 free-swimming
stages (Magalha
˜es 1985). The specimens collected in Sa
˜o Paulo are small to
medium sized animals in which the above morphological characters are not so
clearly visible.
Macrobrachium amazonicum has a native distribution in the coastal river
basins of northern South America (Venezuela to northern Brazil), as well as in
most of the Orinoco, Amazon, Paraguay, and lower Parana
´river basins
(Holthuis 1952, 1966; Rodrı
´guez 1980, 1981; Coelho and Ramos-Porto 1985;
Lo
´pez and Pereira 1996; Pettovello 1996; Magalha
˜es 1999b, 2001). The species
is also present in the northeastern and eastern states of Brazil (Coelho and
Ramos-Porto 1985; Ramos-Porto and Coelho 1990, 1998; Arraes and Ramos-
Porto 1994; Barros and Braun 1997), but their distribution in these states is
1933
probably due to anthropogenic dispersion for aquaculture purposes (Ramos-
Porto and Coelho 1998).
Macrobrachium jelskii (Miers)-Figure 1(3, 4)
Material – Brazil, Sa
˜o Paulo: Rio Tieteˆ Basin, rio Tieteˆ , reservato
´rio de Treˆ s
Irma
˜os, ii.2000–xvi.2000, 44 spec (2 ov. $) (MZUSP 13550); rio Mogi-Guac¸ u,
Barrinha, 2111¢S4809¢W, 12.x.1999, 2 spec. (MZUSP 13101); Rio Tieteˆ
Basin, Pena
´polis (2124¢S5004¢W), 18.xi.2001, 1 ov. $(INPA 888); Pena
´polis
(2124¢S5004¢W), represa Rio Bonito, 29.vii.1995, 57 spec. (INPA 585); idem,
18.xi.1995, 52 spec. (INPA 586); Rio Tieteˆ Basin, represa de Barra Mansa,
Mendonc¸ a (2110’S 4934¢W), 15.xi.2001, 55 spec. (3 ov. $) (INPA 887); Lins,
RPPN Dr. Ivan, 2134¢18¢¢S4938¢19¢¢W, 21.i.2003, 9$(1 ov.) (MZUSP
15575).
Remarks – The telson of M. jelskii always shows a distinct posterior margin,
with a clear descontinuity between the lateral margins and the median point.
The inner pair of spines of the posterior margin, even in adults, is longer than
the median point. The tip of the rostrum is curved upwards, but it is usually
straight over the orbits. Ovigerous females carry few and relatively large eggs;
larvae hatch as benthonic, well advanced form which goes through three stages
until metamorphosis is accomplished (Magalha
˜es 2002).
The distribution of this species is similar to that of M. amazonicum,con-
sidering either natural or anthropogenic dispersal (Holthuis 1952, 1966;
Rodrı
´guez 1980, 1981; Coelho and Ramos-Porto 1985; Ramos-Porto and
Coelho 1990, 1998; Arraes and Ramos-Porto 1994; Lo
´pez and Pereira 1996;
Barros and Braun 1997; Magalha
˜es 1999b, 2001; Collins 2000).
Trichodactylidae H. Milne-Edwards
Dilocarcinus pagei Stimpson-Figure 1(5)
Material – Brazil, Sa
˜o Paulo: Rio Grande, between Mira Estrela and Cardoso,
2001¢51¢¢S5000¢59¢¢W, 23.i.2003, 3 juv., (MZUSP 15581); Rio Turvo, be-
tween Riolaˆ ndia and Cardoso, 2004¢29¢¢S4948¢46¢¢W, 23.i.2003, 1 juv. #2
juv. $(MZUSP 15592); Rio Grande Basin, Coloˆ mbia, 2010¢08.7¢¢S
4836¢83.5¢¢W, 24.vii.2000; 3#(MZUSP 13915); Rio Turvo, between Icem and
Sa
˜oJose
´do Rio Preto, 2025¢07¢¢S4916¢03¢¢W, 23.i.2003, 3 juv. #2 juv. $
(MZUSP 15595); Rio Pardo, between Barretos and Guaı
´ra, 2026¢58¢¢S
4827¢16¢¢W, 24.i.2003, 1 juv. $(MZUSP 15593); Rio Grande Basin, Sa
˜oJose
´
do Rio Preto, ac¸ ude municipal, 2048¢S4922¢W, 12.x.1999, 6#2$(MZUSP
13100); idem, 2#1$(INPA 774); Sa
˜o Jose
´do Rio Preto, represa Rio Preto,
1.viii.1994, 1#(MZUSP 12128); Rio Mogi Guac¸ u Basin, Viradouro, Fazenda
Treˆ s Barras, 2054¢48.9¢¢S4810¢29.6¢¢W, 11.viii.2000, 2#(INPA 872); Vira-
douro, 2055¢35.2¢¢S4810¢28.7¢¢W, 11.viii.2000, 2 #(DZ-USP); Barrinha
(2111’S 4809¢W), rio Mogi-Guac¸ u, 12.x.1999, 2$(MZUSP 13099); idem, 1$
1934
(INPA 773); Barrinha, Rio Mogi-Guac¸ u, 2111¢09¢¢S4810¢35¢¢, 25.i.2003, 6
juv. #(MZUSP 15597). – Parana
´: Rio Paranapanema Basin, Londrina, Faz-
enda Doralice, em lagos, 22.vi.2002, 1 #1$(INPA 894).
Remarks – This crab has a strongly convex carapace in the anteroposterior
direction, with six or, rarely, seven teeth in the anterolateral margins. They are
promptly identified by a distinct transverse carina along the anterior margin of
the third abdominal somite in both males and females. In live specimens, the
carapace is usually bright red. Its distributional range includes the Amazon,
Paraguay and lower Parana
´river basins, from Brazil to Argentina (Bott 1969;
Lopretto 1981; Rodrı
´guez 1992). The above records extend this range to the
upper Parana
´River basin, including the states of Sa
˜o Paulo and Parana
´.
Discussion
Five exotic decapod species are reported in natural environments in the
hydrographic basins of the state of Sa
˜o Paulo (Figure 2), and their occurrence
could be related to different causes. The crayfish Procambarus clarkii has a
worldwide dispersion and Hobbs III et al. (1989) mentioned that introductions
of P. clarkii in Latin America were probably aiming at commercial aquaculture
Figure 2. Map with the distribution of the exotic decapod species recorded in the states of Sa
˜o
Paulo and Parana
´, Brazil. Symbols (solid: occurrence in the wild; open: occurrence in aquaculture
ponds): Procambarus clarkii =.,Macrobrachium amazonicum = , s;Macrobrachium jel-
skii =, ; Macrobrachium rosenbergii = , ; Dilocarcinus pagei = . (Some symbols may
represent more then one locality.)
1935
for United States markets. It appears, however, that this is not the case for
Brazil, where the species apparently has never been commercially reared for
human consumption. Its occurrence in Sa
˜o Paulo is most problably due to its
commercialization as aquarium pet.
In the city of Sa
˜o Paulo, illegal breeding and cultivation of P. clarkii has
been carried out in several technically poorly conceived small-scale domestic
hatcheries in recent years. Juvenile specimens are then sold to local pet shops
where this crayfish species is routinely and openly commercialized. Its occur-
rence in natural environments can possibly be imputed to accidental or even
inconsequent release by regretful aquarium keepers.
The shrimp Macrobrachium rosenbergii was imported to Brazil from
Hawaiian commercial farms in 1977 for aquaculture studies carried out by the
Universidade Federal de Pernambuco (Cavalcanti 1998). M. rosenbergii was
introduced in Sa
˜o Paulo, probably for research purposes, during the early
1980s. During this decade, culture of this species overspread all over the state.
Post-larvae came from local hatcheries and also from the states of Pernam-
buco, Rio de Janeiro, and Espı
´rito Santo. It is certain that M. rosenbergii was
farmed in earthen ponds in all main river basis of the state. Personal infor-
mation (WCV) on sporadic capture of specimens in natural waters has been
made during the past 20 years. However, there is no report on successful
reproduction in the wild.
It seems that there is no well-established population of M. rosenbergii in Sa
˜o
Paulo. One factor that surely contributes to prevent the establishment of this
species in natural waters is the physiological dependence of the larvae to
brackish water (Ling 1969). Currently, all M. rosenbergii farming in operation
in the state of Sa
˜o Paulo are located in river systems that do not drain directly
to the coast. The very large adult male specimen collected in the Tieteˆ River
Basin at Brejo Alegre in 2001 (see Figure 2) had probably escaped accidentally
from a commercial shrimp farm and this escaping may well not have been an
isolated occurrence. However, the direction of flow of the Tieteˆ River water
system is opposite to the coast line, and the system eventually drains into the
Parana
´River.
As opposed to P. clarkii and M. rosenbergii,M. amazonicum,M. jelskii, and
D. pagei are endemic to tropical South America, where they have a wide
geographical distribution. We hypothesize that they are not native to the upper
Parana
´River basin, but were deliberately and or accidentally introduced there.
The presumptive natural distribution of these species includes the Orinoco
(except for D. pagei), Amazon, and Paraguay/lower Parana
´river basins. They
probably evolved in one of these regions after river systems regarded as
ancestral of the western paleo-Amazonas-Orinoco and Parana
´systems were
established along the foreland of the emerging Andes from late Cretaceous/
early Paleocene (for a summary of the history of South American rivers, see
Lundberg et al. 1998). The Amazonian and Paraguay/lower Parana
´decapod
fauna have several common elements, and these species would probably have
dispersed across these paleobasins after subsequent geological events shifted
1936
their boundaries, promoting different sequences of capture of headwater by
one or another basin during Tertiary and Quaternary (Lundberg et al. 1998).
Whereas the Paraguay/lower Parana
´resulted from the uplifting of the Andes
and episodes of marine transgressions and regressions in the latest 90 Myr,
the upper Parana
´has a more ancient origin, probably linked to the South
America/Africa separation during Jurassic-Cretaceous (Stevaux et al. 1997).
The upper Parana
´drains highplain areas of the southern Brazilian Shield, an
ancient Precambrian crystalline basement area in which the sedimentary basin
of the upper Parana
´has been largely non-marine since Triassic (Lundberg et al.
1998). Sedimentological evidences reveal that the paleo-drainage of the Parana
´
Basin during late Cretaceous is similar to that existent today (Fulfaro and
Suguio 1974). Therefore, the two parts of the basin have marked differences in
their geomorphology, limnological, and biotic characteristics (Bonetto 1986a).
Composition of the upper Parana
´aquatic biota is usually very distinct from
that of the rest of the basin, as seen for fishes (Bonetto 1986b; Menezes 1988,
1996; Castro and Menezes 1998), microcrustaceans (Lansac-Toˆ ha et al. 1997),
and decapods (see below), for instance.
Natural dispersion of decapod fauna towards the upper Parana
´would have
been prevented by the Guaı
´ra Falls, a series of imposing falls which marked the
end of the upper course of the Parana
´River (Bonetto 1986a) before it had been
inundated by the artificial reservoir of the Itaipu dam in 1982. Dispersal across
the headwaters of eastern tributaries of the Paraguay River and western trib-
utaries of the upper Parana
´River could also have been avoided by the uplifting
of the Serra de Maracaju during mid-Pliocene (Stevaux 1994; Stevaux et al.
1997). Although M. amazonicum is presently established in some of these
western tributaries of the Parana
´River (Porto 1998) and basin interconnec-
tions are eventually possible during flood season, natural dispersal should not
have occurred through this region due to adverse ecological conditions to these
species, since they are not typical of headwater environments. Indeed, a lon-
gitudinal inventory carried out in the Rio Negro, a eastern tributary of the
Paraguay River, rendered no collections of these species in headwater areas
(Magalha
˜es 2000).
Disregarding possible synonymies and a few doubtful records, and taking
into account only native species in both parts of the basin, there are no com-
mon elements among the decapod fauna recorded for both upper and lower
Parana
´in the historic scientific literature (Ringuelet 1949; Lopretto 1976, 1981,
1998; Boschi 1981; Bisbal 1987; Magalha
˜es and Tu
¨rkay 1996; Pettovello 1996;
Magalha
˜es 2000, 2001; Collins 2000; Collins et al. 2002; see also Magalha
˜es
1999a for other citations). Therefore, the occurrence of M. amazonicum,
M. jelskii,andD. pagei in the upper Parana
´might be considered as the result of
direct (planned or accidental translocations) and/or indirect (displacement of
barriers) antropogenic actions, as discussed below.
The introduction of these two shrimp species in Sa
˜o Paulo was reported by
Machado (1966) and Torloni et al. (1993). Torloni et al. (1993) confirmed that
between 1966 and 1973 M. jelskii (and probably also M. amazonicum) was
1937
introduced in the CESP (Companhia Energe
´tica de Sa
˜o Paulo) pisciculture
stations as part of the transplantation process of the Scianidae fish, Plagioscion
squamosissimus (Heckel), from reservoirs of northeastern Brazil. Commenting
on P. squamosissimus, Torloni et al. (1993) reported that fries escaped to
natural environments in the Rio Pardo in 1970, and later dispersed to the Rio
Grande, reaching the Ilha Solteira and Jupia
´Reservoirs, in the upper Rio
Parana
´, in 1972. Hence, it is reasonable to assume that the freshwater shrimps
could have followed the same pattern of dispersal, as M. amazonicum, which is
currently a well established and abundant species in the upper Rio Parana
´
floodplains (Bialetzki et al. 1997), where the species found thriving ecological
conditions. The presence of M. jelskii in localities of the upper Rio Parana
´
Basin could also have a similar explanation.
Currently, M. amazonicum is experimentally reared in earthen ponds in
Jaboticabal, at the Centro de Aquicultura da UNESP (CAUNESP) (Moraes-
Riodades 2002) and in cages placed in aquaculture ponds in Pindamonhang-
aba, at the Instituto de Pesca de Sa
˜o Paulo. Post-larvae are produced at
hatcheries of the CAUNESP, from broodstock originally brought from the
state of Para
´in 1999 and 2001. These animals have been subjected to very
strong control procedures to avoid accidental dissemination, and post-larvae
are only available for research institutions.
However, M. amazonicum,M. jelskii, and D. pagei may also have been
transplanted to some localities in Sa
˜o Paulo from populations occurring in the
Pantanal region, in the state of Mato Grosso do Sul. Currently, the practice of
‘Pesque & Pague’, which are places for game fishing where people pay by
weight caught, is widespread in the state of Sa
˜o Paulo. Some fish species
captured from natural environments in the Pantanal were sometimes employed
to populate ponds and reservoirs used in such activity. Larvae, juveniles, or
immature forms of decapods may have been transported inadvertently along
with the roots of the aquatic macrophytes, sometimes used as shelter for fish in
containers. The crab D. pagei or the shrimps M. amazonicum and M. jelskii are
very abundant in habitats formed by large patches of aquatic floating vege-
tation, a common feature in the extensive floodplain areas of the Pantanal
(Magalha
˜es 2000) and Paraguay River Basin (Magalha
˜es 2001).
Another likely reason for the establishment of these three species in the
upper Parana
´is the inundation of the Guaı
´ra Falls after formation of the
Itaipu Reservoir in October 1982. The barrier was then displaced 150 km
downriver, allowing possible upstream dispersal of these decapods. The
favorable ecological conditions provided by the lentic environment of the
reservoir and the adjacent floodplain areas of the upper course would have
contributed for a rapid colonization of the region by these species. Such up-
stream dispersal of lower Rio Parana
´faunal components was also verified in
some fish species (Agostinho et al. 1992, 1994).
According to Hobbs III et al. (1989), introductions of P. clarkii have usually
brought negative consequences. Burrowing activity of the species accounts for
damage to levees, dams, and irrigated plantation farms, particularly rice fields,
1938
as well as in pisciculture earthen ponds. Measures for reducing such environ-
mental damages were introduced in California (USA), Spain, and Japan, where
strong pesticides were used in order to eliminate crayfish populations (Huner
2002). Damages associated with the introduction of P. clarkii have been re-
ported, for instance, in Spain (Gutie
´rrez-Yurrita 1998), Portugal (Correia and
Ferreira 1995; Ilhe
´u et al. 2002), Kenya (Mkoji et al. 1999), and Mexico
(Rodrı
´guez-Almaraz and Campos 1994).
The crayfish P. clarkii is well adapted to survive in temporary habitats
(tolerates low oxygen and aerial exposure, persists for extended periods in
burrow systems in the absence of surface waters), lack of larval phase (direct
development), shows rapid growth rates and early sexual maturation (Huner
and Lindqvist 1995). Introduction of this species may cause negative effects to
communities of native aquatic organisms, particularly mollusks, amphibians
and young fishes (Nystro
¨m 2002). Hobbs III et al. (1989) pointed out that
polytrophy makes this crayfish a keystone species in controlling species
composition of aquatic ecosystems.
However, the most problematic aspect of introducing P. clarkii may be
related to the widespread introduction of new diseases to native populations of
aquatic organisms, as it can act as vector for pathogens. Henttonen et al.
(1997) reported the infection of P. clarkii by Psorospermium spp. and Die
´guez-
Uribeondo et al. (1994) showed that the species could be a vector for fungi such
as Saprolegnia parasitica Coker and Aphanomyces astaci Schikora. The latter is
considered a plague, being responsible for the decimation of many crayfish
populations in Spain (Cuellar and Coll 1983), Ireland (Matthews and Reynolds
1992), and Great Britain (Holdich 2000). Although acting as vector for
aphanomycosis, P. clarkii itself is quite resistant to infection (Evans and
Edgerton 2002). Introduction of this species in Brazil may represent a serious
ecological problem, since one of the fungus strains isolated from P. clarkii,is
physiologically adapted to warm waters such as those of tropical and sub-
tropical regions (Die
´guez-Uribeondo et al. 1995). Negative effects on species of
Parastacus, a South American endemic crayfish genus occurring in southern
Brazil, are unknown but could be potentially high, as they may not show
resistance to this plague at all.
M. rosenbergii has been farmed in dozens of other countries in Easter and
Western hemispheres during the past 30 years, but there is little information
about its colonization in natural waters (New et al. 2000). Even so, there are no
reports of any economic damage or environmental impact related to the
introduction of this species (New et al. 2000). Similarly, nothing has been
reported about negative ecological effects associated with the introduction of
M. amazonicum and M. jelskii in northeastern of Brazil during the past
60 years. On the other hand, nothing can be stated about the introduction of
D. pagei because it has been observed only recently.
Hydrographic basins of Sa
˜o Paulo have been suffering from several
anthropogenic interventions that drastically changed the aquatic biota, such as
man-made dams, removal of the riparian vegetation, inappropriate agriculture
1939
practices, contamination by industrial and organic wastes, which increased
siltation, increased suspended material, and caused changes of physical and
chemical parameters of the water (Tundisi et al. 1999). Introduction of an alien
species in a disturbed environment could favor the exotic species over native
ones, by means of predation or competition for niches. Some studies have
shown that privileging endemic or native species in actions for conservation of
natural areas and recovering of disturbed ones is a fundamental aspect for the
maintenance of ecosystem biodiversity and for the better understanding of
their biotic and abiotic interaction processes (Tundisi et al. 1999). The results
presented here suggest that, except for M. rosenbergii, these species may be
established, and indicate that they are probably widely distributed in the upper
Parana
´River drainage. Populational studies should be conducted to corrob-
orate this hypothesis.
Acknowledgments
The authors wish to thank A.A. Agostinho, J.E.P. Cyrino, L.A. Hayd, J.V.
Huner, M.H.A. Leme, G.A.S. Melo, N.A. Menezes, J. Lombardi, L.A.C.
Porto and M.S. Tavares for providing information concerning some issues
discussed in this paper, G. Nakamura for revising the English, and two
anonymous reviewers for helpful suggestions that improved the text. Some of
us (C.M., G.B.B., W.C.V.) thank the Conselho Nacional de Desenvolvimento
Cientı
´fico e Tecnolo
´gico - CNPq for a research grant. Fundac¸ a
˜o de Amparo a
`
Pesquisa do Estado de Sa
˜o Paulo – FAPESP is especially acknowledged for
granting student fellowships (to E.C.M., F.K., H.L.M.S., S.S.R.) and for
providing research funds through the BIOTA/FAPESP Program (Proc. nr. 98/
05073-4).
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