CURRENT DISTRIBUTION OF THE EXOTIC COPEPOD PSEUDODIAPTOMUS TRIHAMATUS WRIGHT , 1937 ALONG THE NORTHEASTERN COAST OF BRAZIL

Instituto Oceanografico da Universidade de Sao Paulo Departamento de Oceanografia Biologica (Praca do Oceanografico 191, 05508-120 Sao Paulo, SP, Brasil) **rmlopes@usp.br The introduction of exotic species is a major cause of depletion and extinction of native populations, a threat only surpassed by habitat destruction (Williamson, 1999). Exotic organisms may inflict negative impact upon native species by several ways, including transmission of pathogens and parasites, genetic degradation, habitat utilization, direct predation or competition for food, and other food web interactions (Williamson, 1996). Aquaculture activities account for a large number of accidental introductions worldwide because of non-intentional releases of small-sized organisms associated with target imported species (Carlton, 1996; Weigle

The introduction of exotic species is a major cause of depletion and extinction of native populations, a threat only surpassed by habitat destruction (Williamson, 1999).Exotic organisms may inflict negative impact upon native species by several ways, including transmission of pathogens and parasites, genetic degradation, habitat utilization, direct predation or competition for food, and other food web interactions (Williamson, 1996).Aquaculture activities account for a large number of accidental introductions worldwide because of nonintentional releases of small-sized organisms associated with target imported species (Carlton, 1996;Weigle et al., 2005).Copepods, like other planktonic organisms, are usually transported as active or dormant stages with breed stocks of fish, shrimps and clams (Reid & Reed, 1994;Saunders, 1993;Saunders et al., 1983).
The planktonic copepod Pseudodiaptomus trihamatus Wright, 1937, native from Indo-Pacific costal waters, was accidentally introduced in Northeast Brazil in 1977 (Medeiros et al., 1991).This species was first encountered in shrimp ponds along the margins of the Potengí River estuary, in the city of Natal.Its presence was attributed to an accidental introduction from a breeder stock of the shrimp Penaeus monodon Fabricius, 1798, imported from Philippines by EMPARN (a State research division dedicated to farming, cattle raising and aquaculture studies) in the same year, because Pseudodiaptomus trihamatus had been recorded in that country (Walter, 1984).No further investigation on this exotic copepod species has been carried out in the Brazilian coast.
In this study we inspected the occurrence of Pseudodiaptomus trihamatus in the Brazilian Northeast coast, from Tamandaré in Pernambuco State to Carutapera in Maranhão STATE, to evaluate whether __________ Contr. No. 874 do Inst. oceanogr. da Usp. or not the species has expanded its distribution range since the early records.Three native species of the same genus were also recorded and their presence compared to P. trihamatus.Additional notes on the salinity ranges of the Pseudodiaptomus species and incidence of associated ectoparasites are also reported here.Annual water temperature in estuaries and coastal waters of the study area is quite constant throughout the year, reaching values from 26 to 30ºC (mean about 27ºC).
Samples were collected at estuaries and inshore waters in the Northeast region by ~50-m long horizontal hauls of a conical plankton net (30-cm diameter, 1.5-m length and 120-µm mesh size), from 2001 to 2005 (Fig. 1).Samples from the Tamandaré region were obtained by using a net trap placed on the sea floor, and applying artificial light as an attraction device.The collected organisms were preserved in 4% formalin neutralized with sodium borate.Zooplankton samples were inspected under a stereomicroscope and all adult Pseudodiaptomus were sorted for further identification.Identification of P. trihamatus was based on the shape of 5 th legs (L5) for males and on the external shape of the genital segment for females, according to Walter (1984;1989).Identification of other Pseudodiaptomus species was based on Björnberg (1981) and Bradford-Grieve et al. (1999).Distinction of Pseudodiaptomus trihamatus from congeneric species previously known for Brazilian waters is easy to perform, as it does not require dissection of specimens during routine zooplankton sorting, except for observation of L5 features in males (Fig. 2).The female genital somite bears two posterolateral spines on the dorsal surface in addition to a ventral pair of long spines, the tip of right spine reaching the margin of the anal somite (Walter, 1984).In addition, females of Pseudodiaptomus spp.so far recorded in Brazil do not carry a centrally positioned, single egg sac as in P. trihamatus.The present investigation confirmed that Pseudodiaptomus trihamatus is widely distributed throughout estuarine and coastal waters off Northeast Brazil (Fig. 1), from Canguaretama in Rio Grande do Norte State (6 o 19'60"S, 35 o 04'08"W) to Barroquinha in Ceará State (3 o 02'12"S, 41 o 24'32"W).We speculate that the documentation of Pseudodiaptomus trihamatus at southern sampling sites 6 and 7 (Fig. 1) might be assigned to a secondary introduction by populations brought along with a stock of Penaeus monodon acquired in 1985 by CAMANOR (a shrimp farm located in Canguaretama, site 7, Fig. 1).The shrimp stock came from a cultivation enterprise situated in Valença, Bahia STATE (at about 13 o S), which imported the exotic shrimp from Taiwan in 1984 (Ana Carolina de B. Guerrelhas, Aquatec Ltda., Canguaretama, RN, Brazil -personal communication), a country where P. trihamatus is known to thrive as a native component of the zooplankton community (Lo et al., 2004).However, after more than 20 years of such a suspected introduction in Bahia State, Pseudodiaptomus trihamatus has not been reported in any area south of Rio Grande do Norte (Medeiros et al., 1991), including the southernmost sites covered by the present investigation (Fig. 1).This particular situation might be attributed either to non-release of the exotic copepod from captivity in Bahia (i.e., efficient management of the imported shrimp stock at that time), or to failure in the establishment of selfreproducing copepod populations in the local environment from released propagules.However, it must be stressed that results of coastal and estuarine zooplankton surveys in Bahia State have not been published during the last 20 years, thus hampering our ability to follow a potential invasive process in that region.It would be highly desirable in future studies to expand the sampling coverage towards southern areas, at least from Rio Grande do Norte to Bahia.
If our southernmost records of Pseudodiaptomus trihamatus are in fact related to a secondary introduction at the Canguaretama site in 1985, then the present expansion of the species towards the northwest could be alternatively ascribed to this southern population, because the Potengí River population has not been tracked by time-series sampling in estuarine waters upon initial detection in shrimp ponds.Molecular biology studies could help to answer whether the present P. trihamatus distribution in Northeast Brazil is due to a single "founder" population or to mixed "seed" populations introduced at different sites and periods.Many notorious invaders (e.g., the zebra mussel in North America) succeed because they have been introduced repeatedly to ideal habitats and have passed through both the 'local dispersal' and 'environment survival and reproduction' filters [sensu Colautti & MacIsaac (2004)].
Other Pseudodiaptomus species occurred simultaneously with P. trihamatus during our survey (Table 1), the most frequent of which was P. acutus (F.Dahl, 1894) (found at 15 sites), followed by P. marshi Wright, 1936 (11 sites) and P. richardi (F.Dahl, 1894) (1 site).Males and females were recorded in all localities.Lower salinity ranges for the genus were relatively similar (18 to 23 psu) in all sampling sites, but maximum salinity values differed widely (Table 1).This result suggests that at least three Pseudodiaptomus species (P.marshi, P. acutus and mainly P. trihamatus) are able to survive and even reproduce (based on presence of ovigerous females) in hypersaline waters (up to 70 psu, in the case of P. trihamatus).Pseudodiaptomus richardi occurred only in the Potengi River estuary during our study, in a narrowed salinity interval not necessarily representative of its natural distribution in Brazilian estuaries (Almeida-Prado Por & Lansac-Tôha, 1984;Lopes, 1994).Tolerance of P. trihamatus to a wide range of salinities seems to confer an additional benefit for successful dispersion of the species in the Northeast coast of Brazil, where artificial salts ponds have been established for both salt and Artemia production (Camara, 1996).Exotic species that are able to survive and disperse are usually highly tolerant to environmental challenges, a competitive advantage over native species (Arthington, 1991).Our sampling effort has not been designed to identify potential ecological impacts of Pseudodiaptomus trihamatus upon other planktonic species.Therefore, we suggest this exotic copepod should be classified as an established species (sensu Williamson & Fitter, 1996), and not as a typical invader [because the latter category implies that some sort of impact is being infringed by the introduced species] until quantitative abundance data and other relevant ecological information is gathered.
Sampling sites where ectoparasites occurred on Pseudodiaptomus spp.are indicated in Table 1.Parasitism by epicarid isopods was rare, both in terms of sampling sites and number of infected individuals.On the other hand, peritrichid ciliates were detected on several copepods (Fig. 2), and interestingly only in estuarine waters.Previous observations (G.F. Medeiros, unpublished data) showed that P. trihamatus collected in shrimp ponds from EMPARN in 1979 were highly infested by the same protozoans, which might suggest a preferential symbiosis between the two species and even a potential "tertiary" introduction of an exotic peritrichid.
In addition to our observations in Piauí and Maranhão States, where the exotic copepod has not been recorded, recent zooplankton studies performed in the vicinities of the Amazon River mouth also failed to detect the species (Magalhães, 2003;Krumme & Liang, 2004).Nevertheless, the expansion of the distributional range of Pseudodiaptomus trihamatus on the North and Northeast coasts of Brazil seems to be an undergoing process, with a potential dispersion trend towards the direction of the Amazon River mouth because of the prevailing northwestward currents.Such scenario demands a long-term monitoring program of exotic planktonic organisms in the region, if we want to understand and develop management practices to control their potential impacts on native aquatic species.

Fig. 1 .
Fig. 1.Localities along the Northeastern coast of Brazil where zooplankton samples were taken for the assessment of Pseudodiaptomus trihamatus distribution during 2001-2005.

Table 1 .
Sampling sites and periods, salinity data (for either estuarine or coastal waters) and presence of parasites on adult Pseudodiaptomus spp.recorded on the Northeastern Brazilian coast.Presence of copepods is indicated by + and absence by -