Population genetic structure of Brazilian shrimp species (Farfantepenaeus sp., F. brasiliensis, F. paulensis and Litopenaeus schmitti: Decapoda: Penaeidae)

EVOLUTIONARY GENETICS

RESEARCH ARTICLE

Population genetic structure of Brazilian shrimp species (Farfantepenaeus sp., F. brasiliensis, F. paulensis and Litopenaeus schmitti: Decapoda: Penaeidae)

Jaqueline Gusmão^{I, II}; Cristiano Lazoski^II; Antonio M. Solé-Cava^{II, III}

^IUniversidade Estadual do Rio de Janeiro, Instituto de Biologia Roberto Alcântara Gomes, Departamento de Biologia Celular e Genética, Rio de Janeiro, RJ, Brazil

^IIUniversidade Federal do Rio de Janeiro, Instituto de Biologia, Departamento de Genética, Laboratório de Biodiversidade Molecular, Rio de Janeiro, RJ, Brazil

^IIIUniversity of Liverpool, Department of Environmental and Evolutionary Biology, Port Erin Marine Laboratory, Isle of Man, United Kingdom

^{Correspondence}

ABSTRACT

Penaeid shrimps are important resources for worldwide fisheries and aquaculture. In the Southwest Atlantic, Farfantepenaeus brasiliensis, F. paulensis, F. subtilis, Farfantepenaeus sp. and Litopenaeus schmitti are among the most important commercially exploited species. Despite their high commercial value, there is little information available on the different aspects of their biology or genetics and almost no data on their stock structure. We used allozymes to estimate variability levels and population genetic structure of F. brasiliensis, F. paulensis, L. schmitti and the recently detected species Farfantepenaeus sp. along as much as 4,000 km of Brazilian coastline. No population heterogeneity was detected in F. brasiliensis or L. schmitti along the studied area. In contrast, F_ST values found for Farfantepenaeus sp. and F. paulensis indicate that the populations of those two species are genetically structured, comprising different fishery stocks. The largest genetic differences in F. paulensis were found between Lagoa dos Patos (South) and the two populations from Southeast Brazil. In Farfantepenaeus sp., significant differences were detected between the population from Recife and those from Fortaleza and Ilhéus.

Key words: Farfantepenaeus, Litopenaeus, allozymes.

Introduction

Penaeid shrimps are important resources for worldwide fisheries and aquaculture (Sunden and Davis, 1991). Population genetics have proven valuable for estimating stock boundaries and genetic variability of wild shrimp populations for fisheries (Benzie, 2000).

Along the Brazilian coast, juvenile shrimps are caught in natural nursery areas by small vessels, while the commercial fleet harvest adult populations in the open sea (Valentini et al., 1991). As a result of the unrestricted past growth of the industrial fleet, of the increased number of small boats fishing in natural nurseries and estuaries and of environmental degradation, there is evidence of declining stocks of shrimps along the Brazilian coast. Farfantepenaeus brasiliensis, F. paulensis, F. subtilis and Litopenaeus schmitti are among the main commercially important Brazilian species (Neto, 1991; Valentini et al., 1991). Populations of F. brasiliensis and F. paulensis of the South/Southeast regions showed a decrease of 87.1% in relative stock abundance between 1965-1994 (Neto and Dornelles, 1996). A decline was also observed in populations of F. subtilis (Neto, 1991) and L. schmitti (Neto and Dornelles, 1996). Despite their high commercial value and the need to understand their stock structure, so that effective management measures can be applied, there is still little information available on their population genetics (the sole exception is the analysis of F. paulensis in the South of Brazil; Delevedove, 1996), and even the taxonomic status of some species has just recently been clarified. Genetic analyses revealed a new (cryptic) Brazilian species of Farfantepenaeus (Farfantepenaeus sp.; formerly Penaeus subtilis¹) ranging from Rio de Janeiro to Northeast Brazil, showing that Penaeus subtilis (sensu Pérez Farfante, 1969) was in fact a mixture of two different species (Gusmão et al., 2000; Maggioni et al., 2001).

In this paper we used allozymes to estimate the variability levels and the population genetic structure of four Brazilian species, F. brasiliensis, F. paulensis, L. schmitti and the new species, Farfantepenaeus sp., over a distance of approximately 4,000 km of coastline.

Different stocks were observed within populations of F. paulensis and of Farfantepenaeus sp., while no detectable heterogeneity could be observed for populations of F. brasiliensis and L. schmitti along the studied area.

Material and Methods

We collected 556 individuals of F. brasiliensis, F. paulensis, L. schmitti and Farfantepenaeus sp. from eight different sites along 4,000 km of Brazilian coastline, between October 1997 and September 1999. Sampling localities are indicated in Figure 1. Samples were stored on dry ice and transported to the laboratory where they were identified morphologically according to Pérez Farfante (1969). Muscle tissue was preserved in liquid nitrogen until required for allozyme analysis.

Horizontal 12.5% starch gel electrophoresis was carried out as previously described (Murphy et al., 1990; Gusmão et al., 2000). The 11 enzyme systems investigated are shown in Table 1. Allozyme patterns were visualised using standard enzyme stains (Manchenko, 1994). Genotype frequencies were used to estimate gene frequencies, heterozygosities, tests for Hardy-Weinberg equilibrium, and inbreeding indices, using the BIOSYS-1 programme version 1.7 (Swofford and Selander, 1981). The significance of F_IS (H_o: F_IS = 0) and F_ST (H_o: F_ST = 0) were tested according to Waples (1987).

The mean number of migrants (N_em; Wright, 1978) between populations was estimated as N_em » (1/F_ST)-1)/4. There have been concerns about the direct use of F_ST to estimate gene flow (Whitlock and McCauley, 1999). However, F_ST remains a robust estimate of multi-population differentiation when the number of loci analysed is not small (Neigel, 2002), so we chose to use it to facilitate comparison with data from the literature. We used a Mantel test (Sokal and Rohlf, 1995), between pairs of Farfantepenaeus and Litopenaeus populations, with 1000 replicates, to verify if geographic distances could be correlated to genetic distances.

Results and Discussion

The four species studied had distinct population structure patterns. Populations of Farfantepenaeus brasiliensis and Litopenaeus schmitti did not show any significant structuring (F_ST = 0.011 and 0.024, respectively; c² test (Waples, 1987) null hypothesis: F_ST = 0; p > 0.05) along the studied area. In contrast, the null hypothesis of panmixia was rejected (p < 0.005) for populations of Farfantepenaeus sp. (F_ST = 0.032; N_em = 5.31) and F. paulensis (F_ST = 0.045; N_em = 7.56; Table 2).

The mean value of F_ST observed for the Brazilian populations of L. schmitti (F_ST = 0.024) is within the range reported for Cuban populations of the same species, using allozymes (F_ST = 0.021-0.038) and microsatellites (F_ST = 0.005-0.060; Espinosa et al., 2002). High genetic homogeneity has been reported for many other penaeid species (reviewed in Benzie, 2000).

The high F_ST values found for Farfantepenaeus sp. and F. paulensis, even over shorter distribution ranges and using the same allozyme systems employed for F. brasiliensis and L. schmitti, indicate that the populations of those two species are genetically structured (p < 0.005). Pair-wise comparisons of the populations (contingency c², Table 2) show that the largest population differences in F. paulensis were found between Lagoa dos Patos (South) and the two populations from Southeast Brazil (p < 10^-4). In Farfantepenaeus sp., significant differences were detected between the population from Recife and those from Fortaleza (c² = 27.49; p < 0.05) and Ilhéus (c² = 30.57; p < 0.01). Similar levels of population genetic structuring have also been observed for several species, e.g., Australian populations of Penaeus monodon (Benzie et al., 1992) and of Melicertus latisulcatus (Mulley and Latter, 1981); populations of M. kerathurus from the Mediterranean (Mattoccia et al., 1987); Cuban populations of F. notialis (Espinosa et al., 1996; García-Machado et al., 2001); and Californian populations of L. stylirostris (Aubert and Lightner, 1999; De La Rosa-Velez et al., 2000; Ramos-Paredes and Grijalva-Chon, 2003) and of F. californiensis (De La Rosa-Velez et al., 2000).

Mean heterozygosity values observed for Brazilian species (H = 0.02-0.10) were similar to those reported in other surveys (H = 0.006-0.175) (Benzie, 2000; García-Machado et al., 2001; Espinosa et al., 2002; Ramos-Paredes and Grijalva-Chon, 2003). The Mpi locus showed a relatively high variability among Farfantepenaeus species. This could be related to its tertiary structure (Solé-Cava and Thorpe, 1989) or to some hitherto unknown balanced selection regime acting on that locus. Gene frequencies at the 14 loci analysed, and mean heterozygosity values for each population are shown in Table 3.

Significant deviations from Hardy-Weinberg expectations (heterozygote deficiencies, p < 0.05; Fisher's exact test, corrected with Bonferroni series; Lessios, 1992) were found for the Pgm-1 locus in two populations of F. paulensis. Heterozygote deficiencies are common in marine invertebrates (Hare et al., 1996), and could indicate population mixing or a number of actual or artifactual factors (Zouros and Foltz, 1984).

In the same way as observed here, levels of worldwide genetic population structure vary widely between different species of shrimp, so that populations separated by thousands of kilometres can be genetically more similar than others over very short distances (Benzie, 2000). Some authors have suggested that differences between species in levels of genetic variation and genotype distribution might be related to life history types (Mulley and Latter, 1981; De La Rosa-Velez et al., 2000). Recently, a major survey of published data indicates that historical events, over large biogeographic scales, may explain the patterns observed better than present day dispersal (Benzie, 2000).

The genetic structure observed in wild populations of F. notialis (Espinosa et al., 1996; García-Machado et al., 2001), F. californiensis and of L. stylirostris (De La Rosa-Velez et al., 2000) as well as those described here for the Brazilian populations of F. paulensis and Farfantepenaeus sp., does not seem to reflect large biogeographical events but, rather, patterns of present day dispersal. In Cuba, for example, the genetic differences detected between populations of F. notialis collected in the Batabanó and the Ana María Gulfs, which are less than 15 km apart, could be due to localized recruitment or to temporal variation in allele frequencies (García-Machado et al., 2001). These factors could be directly or indirectly related to the presence of the Calzones Gulf (the deepest in Cuba), which might prevent the movement of larvae and adults.

Further evidence that the patterns of differentiation observed are more likely to reflect present day dispersal, rather than biogeographical patterns in the Brazilian shrimp populations, is that in spite of their different levels of population structuring, the species studied here have quite similar distribution ranges. The two species that did not present any significant population differentiation F. brasiliensis and L. schmitti occur from the South of Brazil to the Caribbean, and have wide overlapping zones with the distributions of F. paulensis, in the South of Brazil, and of Farfantepenaeus sp. in Southeast and Northeast Brazil. Thus, the incongruence found between their population structure patterns cannot be attributed to common biogeographic boundaries. Moreover, the observed levels of differentiation among populations of F. paulensis and of Farfantepenaeus sp. do not seem to indicate a direct correlation with geographic distances (Mantel test, p > 0.05).

Instead of biogeographic factors, the observed differences in population structure between the four species studied seem to reflect the differences in their biology. Among Brazilian shrimp species, the periods of reproduction, estuary post-larvae penetration and sub-adult emigration vary depending on the species and even among populations of the same species in different geographical regions (reviewed in Gusmão, 2001). Differences in environmental preferences in relation to water temperature, salinity, sediment type and bathymetry are also observed among species (Holthuis, 1980; Paiva, 1997). For example, F. paulensis is found in cold waters where spawning occurs, usually below 50 m depth, and its migration is more related to depth than to latitude (Zenger and Agnes, 1977). F. brasiliensis and L. schmitti, on the other hand, prefer warmer waters, so that the migration of F. brasiliensis is more related to latitude (Zenger and Agnes, 1977).

F. paulensis ranges from Cabo Frio (Rio de Janeiro State - RJ), along the continental shelves of Brazil and Uruguay, to northeast Argentina (Pérez Farfante, 1969; Holthuis, 1980). The main F. paulensis offshore fishing area is located between Santos (São Paulo State - SP) and Torres (Rio Grande do Sul State - RS) (Iwai, 1973), but there are two major adult congregation zones: one off Santa Catarina State (SC), and the second between Santos and São Sebastião Island (littoral North of SP; Figure 1) (Zenger and Agnes, 1977; Melquíades, 1997). Important juvenile shrimp populations can be found in the estuaries of Rio Grande do Sul, but no adult breeding grounds are found in the offshore waters of Rio Grande do Sul or Uruguay (Iwai, 1973; Zenger and Agnes, 1977). Data on coastal currents, wind direction and velocity between Florianópolis (SC) and Laguna de Castillo (Uruguay) indicate that the post larvae that populate nursery areas of Lagoa dos Patos and Uruguay may originate in the breeding grounds off Santa Catarina State (D'Incao, 1991). This hypothesis obtained further support from an allozyme study that indicated a high level of genetic homogeneity between populations from both areas (Delevedove, 1996).

The present study shows that the populations of F. paulensis from Rio de Janeiro and Santos (Southeast of Brazil) are significantly different from that from Lagoa dos Patos (South). Thus, it is possible that the structuring pattern observed for F. paulensis reflects the presence of two breeding populations (stocks) concentrated in different geographic areas along the species range. The South-eastern stock comprises the shrimps living in the Santos/ Rio de Janeiro area, and the Southern stock the shrimps from Santa Catarina/Lagoa dos Patos, and perhaps Uruguay.

Unfortunately, there is little information about the biology of Farfantepenaeus sp. species, which makes discussing the possible causes of the observed population heterogeneity difficult. In addition, the available information to date is based on the overlap of data about the cryptic species F. subtilis and Farfantepenaeus sp. (Gusmão et al., 2000). Nevertheless, despite the factors responsible for the observed structuring patterns, the fact that genetically distinct populations exist in Farfantepenaeus sp. and F. paulensis is clear, and should be taken into account for future aquaculture programs and fisheries management of both resources.

Acknowledgments

The authors would like to thank E. Araújo, F. D'Incao, L. Weber, P. Paiva and P. Vianna for help with collecting the samples and G. Solha for technical assistance. This work was supported by grants from CAPES, CNPq, FAPERJ, FUJB and PADCT (Brazil).

Received: September 25, 2003; Accepted: July 19, 2004.

Associate Editor: João S. Morgante

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1

In a recent review, the subgenera Farfantepenaeus and Litopenaeus, formerly grouped under the Penaeus genus, were raised to generic level (Pérez Farfante and Kensley, 1997).

Publication Dates

• Publication in this collection
  08 Sept 2005
• Date of issue
  Mar 2005

History

• Received
  25 Sept 2003
• Accepted
  19 July 2004