Abundance and spatial-temporal distribution of the shrimp Xiphopenaeus kroyeri (Decapoda: Penaeidae): an exploited species in southeast Brazil

Abundância e distribuição espaço-temporal do camarão Xiphopenaeus kroyeri (Decapoda: Penaeidae): uma espécie em explotação no sudeste do Brasil

E. R. Silva G. S. Sancinetti A. Fransozo A. Azevedo R. C. Costa About the authors

Abstract

This study evaluated the abundance and spatial-temporal distribution of the shrimp Xiphopenaeus kroyeri in the coastal region of Macaé, state of Rio de Janeiro, southeastern Brazil. Monthly samples were obtained from March 2008 to February 2010 in six stations located in Inner (5, 10 and 15m depth) and Outer (25, 35 and 45m depth) areas. It was used a commercial fishery boat equipped with an otter-trawl net (3.5 m mouth width, mesh size 20mm and 15mm in the cod end). Water samples were taken for determination of temperature and salinity, and sediment samples for determination of texture and organic matter content. A total of 7146 shrimps were sampled. About 95% of all shrimps were caught in the shallow area, i.e., depths <20m. Greatest abundances were recorded in winter and spring. No significant correlation was observed between sediment (phi) and abundance. The distribution of X. kroyeri in the studied area was closely related to seasonal cold waterfront of the South Atlantic Central Water (SACW) and temperature was the main factor affecting the species abundance.

Keywords:
abundance; abiotic factors; Penaeidae; SACW

Resumo

Este estudo avaliou a abundância e a distribuição espaço–temporal do camarão Xiphopenaeus kroyeri na área costeira da região de Macaé, estado do Rio de Janeiro no sudeste do Brasil. As coletas foram realizadas mensalmente de março de 2008 a fevereiro de 2010 em seis transectos localizados na área interna (5, 10 e 15m profundidade) e na área externa (25,35 e 45m profundidade). Foi utilizado um barco de pesca comercial equipado com uma rede de arrasto tipo otter-trawl (3,5m abertura de boca, 20mm de malha e 15mm de ensacador). Foram obtidas amostras de água para determinação da temperatura e da salinidade e amostras de sedimento para determinação da granulometria e teor de matéria orgânica. Um total estimado de 7146 camarões foi amostrado. Aproximadamente, 95% de todos os camarões foram capturados “Inner Area”, ou seja, profundidades <20m. As maiores abundâncias foram registradas no inverno e na primavera. Não houve correlação significativa entre o sedimento (phi) e abundância. De acordo com os resultados deste estudo, a distribuição do X. kroyeri na área de estudo está intimamente ligada à sazonalidade da frente térmica da ACAS e a temperatura é o principal fator que afetou a abundância da espécie.

Palavras-chave:
abundância; fatores abióticos; Penaeidae; ACAS

1 Introduction

The shrimp Xiphopenaeus kroyeri iis restrict to the Western Atlantic, from North Carolina (United States) to Santa Catarina (south Brazil) (Holthuis, 1980HOLTHUIS, L.B., 1980. Shrimps and prawns of the world: An annotated catalogue of species of interest to fisheries. Rome: FAO, 125 p. Fisheries Synopsis.), although there are records of its occurrence in Virginia (United States)and Rio Grande do Sul (Brazil) (D’Incao et al., 2002D’Incao, F., Valentini, H. and RODRIGUES, L.F., 2002. Avaliação da pesca de camarões nas regiões sudeste e sul do Brasil: 1965-1999. Atlantica, vol. 24, pp. 103-116.). In general, it lives exclusively in the marine environment throughout its life cycle, and its greatest abundances are reported in shallow depths (<30m) (Boschi, 1963BOSCHI, E.E., 1963. Los camaronês comerciales de la família Penaeidae de lacosta Atlántica de América delSur. Boletim do Instituto de Biologia Marinha, vol. 3, pp. 1-39.). This specie is an important fishery resource globally (Gillett, 2008Gillett, R., 2008. Global study of shrimp fisheries. Rome: FAO, 475 p. Fisheries Technical Paper.) and the second most important fishery resource in southeastern Brazil (Castro et al., 2005CASTRO, R.H., COSTA, R.C., FRANSOZO, A. and MANTELATTO, F.L.M., 2005. Population structure of seabob shrimp Xiphopenaeus kroyeri (Heller, 1862) (Crustacea: Penaeoidea) in the littoral of São Paulo, Brazil. Scientia Marina, vol. 69, pp. 105-112.). The Southeastern-South Brazilian continental shelf suffers with high levels of extraction by artisanal and industrial fisheries, with main targeted species including the most profitable shrimp species such as the pink shrimp Farfantepenaeus brasiliensis (Latreille, 1817) and F. paulensis (Pérez Farfante, 1967), the white shrimp Litopenaeusschimitti (Burkenroad, 1936) and the Atlantic seabob shrimp Xiphopenaeu skroyeri (Heller, 1862) (Valentini et al., 1991aValentini, H., D’Incao, F., RODRIGUES, L.F., REBELONETO, J.E. and DOMIT, L.G., 1991a. Análise da pesca do camarãosete-barbas (Xiphopenaeus kroyeri) nas regiões sudeste e sul do Brasil. Atlantica, vol. 13, no. 1, pp. 171-178., bValentini, H. and D’Incao, F., RODRIGUES, L.F., REBELONETO, J.E. and RAHN, E., 1991b. Análise da pesca do camarão-rosa (Penaeus brasiliensis e P. paulensis) nas regiões sudeste e sul do Brasil. Atlântica, vol. 13, no. 1, pp. 143-158.; D’Incao et al., 2002D’Incao, F., Valentini, H. and RODRIGUES, L.F., 2002. Avaliação da pesca de camarões nas regiões sudeste e sul do Brasil: 1965-1999. Atlantica, vol. 24, pp. 103-116.; Branco, 2005Branco, J.O., 2005. Biologia e pesca do camarão sete-barbas (Heller) (Crustacea, Penaeidae), na Armação do Itapocoroy, Penha, Santa Catarina, Brasil. Xiphopenaeus kroyeriRevista Brasileira de Zoologia, vol. 22, no. 4, pp. 1050-1062. http://dx.doi.org/10.1590/S0101-81752005000400034.
http://dx.doi.org/10.1590/S0101-81752005...
; Costa et al., 2005COSTA, R.C., FRANSOZO, A., CASTILHO, A.L. and FREIRE, F.A.M., 2005. Annual, seasonal and spatial variation of abundance of . Artemesia longinaris (Decapoda, Penaeoidea) in a region a southeastern region of BrazilJournal of the Marine Biological Association of the United Kingdom, vol. 85, no. 1, pp. 107-112. http://dx.doi.org/10.1017/S0025315405010908h.
http://dx.doi.org/10.1017/S0025315405010...
).Due to this intense commercial exploitation, in the last few years there has been a decline in shrimp natural stocks (IBAMA, 2006INSTITUTO BRASILEIRO DO MEIO AMBIENTE E DOS RECURSOS NATURAIS RENOVÁVEIS – IBAMA. Centro Nacional de Pesquisa e Conservação da Biodiversidade Marinha do Sudeste e Sul – CEPSUL, 2006. Relatório da reunião técnica de análise da pescaria do camarão sete-barbas (Xiphopenaeus kroyeri). Itajaí: Ministério do Meio Ambiente.; Vasconcellos et al., 2007VASCONCELLOS, M., DIEGUES, A.C. and SALLES, R.R., 2007. Limites e gestão da pesca artesanal costeira. In: A.L. COSTA, ed. Nas redes da pesca artesanal. Brasília: PNUD/ IBAMA, pp. 15-83.).

Xiphopenaeus kroyeri is classified by the Brazilian government as overfished (Brasil, 2004BRASIL. Ministério do Meio Ambiente – MMA, 2004. Instrução Normativa n° 5, de 21 de maio de 2004. Dispõe sobre espécies ameaçadas de extinção e espécies sobreexploradas ou ameaçadas de sobreexploração, os invertebrados aquáticos e peixes. Diário Oficial da União, Brasília, 28 maio.). Therefore, ecological studies about this species, including fishing grounds, are extremely relevant for proposing adequate conservation and management measures.

Ecological studies concerning crustaceans were conducted in southeastern Brazil (Fransozo et al., 2002Fransozo, A., COSTA, R.C., MANTELATTO, F.L.M., PINHEIRO, M.A.A. and SANTOS, S., 2002. Composition and abundance of shrimp species (Peneidea and Caridea) in Fortaleza bay, Ubatuba, São Paulo, Brazil. In: E. ESCOBAR-BRIONES and F. ALVAREZ, eds. Modern approaches to the study of crustacea. Dordrecht: Kluwer Academic Publishers, pp. 117-125.; Castro et al., 2005CASTRO, R.H., COSTA, R.C., FRANSOZO, A. and MANTELATTO, F.L.M., 2005. Population structure of seabob shrimp Xiphopenaeus kroyeri (Heller, 1862) (Crustacea: Penaeoidea) in the littoral of São Paulo, Brazil. Scientia Marina, vol. 69, pp. 105-112.; Costa et al., 2007COSTA, R.C., FRANSOZO, A., FREIRE, F.A.M. and CASTILHO, A.L., 2007. Abundance and ecological distribution of the “sete-barbas” shrimp Xipohpenaeuskroyeri(Heller, 1862) (Decapoda: Penaeoidea) in three bays of the Ubatuba region, South-eastern Brazil. Gulf and Caribbean Research, vol. 19, pp. 33-41., 2011COSTA, R.C., HECKLER, G.S., SIMÕES, S.M., LOPES, M. and CASTILHO, A.L., 2011. Seasonal variation and environmental influences on abundance of juveniles of the seabob shrimp Xiphopenaeus kroyeri (Heller, 1862) in southeastern Brazil. In: D. PESSANI, C. FROGLIA, E. BIAGGI, N. NURRA, R. BASILI, S. BONELLI, E. GAVETTI, R.M. SARTOR, G. RAPPINI, T. TIRELLI, eds. Behaviour, ecology, fishery. Turin: Museo Regionale di Scienze Naturali di Torino, pp. 45-56.; Almeida et al. 2012bAlmeida, A.C., Fransozo, A., Teixeira, G.M., Hiroki, K.A.N., Furlan, M. and Bertini, G., 2012b. Ecological distribution of the shrimp (Crustacea: Decapoda: Caridea) in three bays on the south-eastern coast of Brazil. Nematopalaemon schmittiAfrican Journal of Marine Science, vol. 34, no. 1, pp. 93-102. http://dx.doi.org/10.2989/1814232X.2012.673292.
http://dx.doi.org/10.2989/1814232X.2012....
; Heckler et al., 2013Heckler, G.S., Simões, S.M., Santos, A.P.F., Fransozo, A. and Costa, R.C., 2013. Population dynamics of the seabob shrimp Xiphopenaeus kroyeri (Dendrobranchiata, Penaeidae) in south-eastern Brazil. African Journal of Marine Science, vol. 35, no. 1, pp. 17-24. http://dx.doi.org/10.2989/1814232X.2013.769901.
http://dx.doi.org/10.2989/1814232X.2013....
; Silva, 2013SILVA, E.R., 2013. Dinâmica Populacional do Camarão Sete-Barbas Xiphopenaeus kroyeri (Heller, 1862) (Decapoda: Penaeoidea) no Litoral de Macaé-RJ. Macaé: Universidade Federal do Rio de Janeiro, 112 p. Masters Dissertation in Biology.), principally on the coast of São Paulo. However, they are scarce on the coast of Rio de Janeiro, especially on the study region, Santana Archipelago, in Macaé (RJ).

The region studied here is a multiple-use Marine Protect Area. Protect Areas constitute a clearly defined geographical space, recognized, dedicated and managed, through legal or other effective means, to achieve the long-term conservation of nature with associated ecosystem services and cultural values (Dudley, 2008Dudley, N., 2008. Guidelines for applying protected area management categories. Gland: IUCN. 86 p.). This new overall IUCN protected area definition supersedes the 1999 Marine Protect Areas (MPAs) definition in marine areas.

The multiple-use MPA of Santana Archipelago is localized in a region with peculiar characteristics due to the dynamics of water masses and upwelling event that provides an increase in the concentration of nutrients in the water and thus increases the primary productivity. Despite the peculiarities, only the studies of Semensato and Di Beneditto (2008)Semensato, X.E.G. and DI BENEDITTO, A.P.M., 2008. Population dynamic and reproduction of (Decapoda, Penaeidae) in Rio de Janeiro State, South-eastern Brazil. Artemesia longinarisBoletim do Instituto de Pesca, vol. 34, pp. 89-98. and Sancinetti at al. (2014SANCINETTI, G.S., AZEVEDO, A., CASTILHO, A.L., FRANSOZO, A. and COSTA, R.C., 2014. How marine upwelling influences the distribution of Artemesia longinaris (Decapoda: Penaeoidea)? Latin American Journal of Aquatic Research, vol. 42, no. 2, pp. 322-331., 2015Sancinetti, G.S., Azevedo, A., Castilho, A.L., Fransozo, A. and Costa, R.C., 2015. Population biology of the commercially exploited shrimp Artemesia longinaris (Decapoda: Penaeidae) in an upwelling region in the Western Atlantic: comparisons at different latitudes. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 75, no. 2, pp. 305-313. http://dx.doi.org/10.1590/1519-6984.11813. PMid:26132012.
http://dx.doi.org/10.1590/1519-6984.1181...
) focusing on the reproduction of Artemesia longinaris Spence Bate, 1888 were performed in the region.

The establishment of an effective system of protected areas composes the global strategy for the conservation of biodiversity. The spread of the concept that aquatic protected areas are essential for biodiversity conservation of the oceans and continental waters is increasing, allying itself, in the 90s, the idea of that are essential to maintaining the fishery yield (Dayton et al. 2000DAYTON, P.K., SALA, E., TEGNER, M.J. and THRUSH, S., 2000. Marine reserves: parks, baselines and fishery enhancement. Bulletin of Marine Science, vol. 66, no. 3, pp. 617-634.; Hyrenbach et al., 2000HYRENBACH, K.D., FORNEY, K.A. and DAYTON, P.K., 2000. Marine protected areas and ocean basin management. Aquatic Conservation: marine and freshwater ecosystems, vol. 10, pp. 437-458.; Halpern and Warner, 2002Halpern, B.S. and Warner, R.R., 2002. Marine reserves have rapid and lasting effects. Ecology Letters, vol. 5, no. 3, pp. 361-366. http://dx.doi.org/10.1046/j.1461-0248.2002.00326.x.
http://dx.doi.org/10.1046/j.1461-0248.20...
; Gell and Roberts, 2003Gell, F.R. and Roberts, C.M., 2003. Benefits beyond boundaries: the fishery effects of marine reserves. Trends in Ecology & Evolution, vol. 18, no. 9, pp. 448-455. http://dx.doi.org/10.1016/S0169-5347(03)00189-7.
http://dx.doi.org/10.1016/S0169-5347(03)...
; Brasil, 2007BRASIL. Ministério do Meio Ambiente – MMA, 2007. Áreas aquáticas protegidas como instrumento de gestão pesqueira. Brasília: Ministério do Meio Ambiente. pp. 4-13. Série Áreas Protegidas do Brasil, 4.). Several authors have stated that the establishment of these protected areas is an excellent instrument for recovery threatened or collapsed stocks (Bohnsack, 1998BOHNSACK, J.A., 1998. Marine reserves, zoning and the future of fisheries management. Fisheries (Bethesda, Md.), vol. 21, no. 9, pp. 14-16.; Ferreira and Maida, 2001Ferreira, B.P. and Maida, M., 2001. Fishing and the future of Brazil’s Northeastern reefs. Integrated Coastal Zone and Shelf-Sea Research, vol. 38, pp. 22-23.; Lubchenco et al., 2003Lubchenco, J., PALUMBI, S.R., GAINES, S.D. and ANDELMAN, S., 2003. Plugging the hole in the ocean: the emerging science of marine reserves. Ecological Application, vol. 13, no. 1, suppl, pp. S3-S7.; Russ and Alcala, 2011Russ, G.R. and Alcala, A.C., 2011. Enhanced biodiversity beyond marine reserves boundaries: the cup spillith over. Ecological Applications, vol. 21, no. 1, pp. 241-250. http://dx.doi.org/10.1890/09-1197.1. PMid:21516901.
http://dx.doi.org/10.1890/09-1197.1...
; Almeida et al., 2012aAlmeida, A.C., Baeza, J.A., Fransozo, V., Castilho, A.L. and Fransozo, A., 2012a. Reproductive biology and recruitment of . Xiphopenaeus kroyeri in a marine protected area in the Western Atlantic: implications for resource managementAquatic Biology, vol. 17, no. 1, pp. 57-69. http://dx.doi.org/10.3354/ab00462.
http://dx.doi.org/10.3354/ab00462...
).

The aim of this study is to analyze the influence of the depth and abiotic factors (temperature, salinity, texture and organic matter content of sediment) on the abundance and spatial and temporal distribution of X. kroyeri in the study region.

2 Material and Methods

Samples were obtained monthly from March 2008 to February 2010 in Macaé, state of Rio de Janeiro (22° 22’ 33” S and 41° 46’ 30” W), in the Marine Protect Area of Santana Archipelago. According to Castro-Filho et al. (1987)CASTRO-FILHO, B.M., MIRANDA, L.B. and MIYAO, S.Y., 1987. Condições hidrográficas na plataforma continental ao largo de Ubatuba: variações sazonais e em média escala. Boletim do Instituto Oceanográfico da Universidade de São Paulo, vol. 35, no. 2, pp. 135-151., the region of Macaé is influenced by the oceanic currents of Brazil (T>20°C, S>36) and Malvinas (T<15°C, S< 34). Due to the confluence of both currents between latitudes 25°S and 45°S of the Western South Atlantic observed in certain periods of the year, there is the formation of water masses like the South Atlantic Central Water (SACW: T<20°C, S<36.4), accounting for part of the convergence of the subtropical gyre and giving rise to the Cabo Frio upwelling, which extends between latitudes 23°S e 29°S (Campos et al., 1996Campos, E.J.D., Ikeda, Y., Castro, B.M., Gaeta, S.A., Lorenzzetti, J.A. and Stevenson, M.R., 1996. Experiment studies circulation in the western South Atlantic. Eos, Transactions, American Geophysical Union, vol. 77, no. 27, pp. 253-259. http://dx.doi.org/10.1029/96EO00177.
http://dx.doi.org/10.1029/96EO00177...
, 2000Campos, E.J.D., Velhote, D. and da Silveira, I.C.A., 2000. Shelf break upwelling driven by Brazil Current cyclonic meanders. Geophysical Research Letters, vol. 27, no. 6, pp. 751-754. http://dx.doi.org/10.1029/1999GL010502.
http://dx.doi.org/10.1029/1999GL010502...
; Silveira et al., 2000SILVEIRA, I.C.A., SCHMIDT, A.C.K., CAMPOS, E.J.D., GODOI. S.S. and IKEDA, Y., 2000. A Corrente do Brasil ao largo da costa leste brasileira. Boletim do Instituto Paulista de Oceanografia, vol. 48, no. 2, pp. 171-183.; Acha et al., 2004Acha, E.M., Mianzan, H.W., Guerrero, R.A., Favero, M. and Bava, J., 2004. Marine fronts at the continental shelves of austral South America physical and ecological processes. Journal of Marine Systems, vol. 44, no. 1-2, pp. 83-105. http://dx.doi.org/10.1016/j.jmarsys.2003.09.005.
http://dx.doi.org/10.1016/j.jmarsys.2003...
). This upwelling is enhanced by coastal winds and by the break of the continental shelf (approximately 50 km) driven by the meandering pattern and eddy of the Current of Brazil (Castro and Miranda, 1998Castro, B.M. and MIRANDA, L.B., 1998. Physical oceanography of the western Atlantic continental shelf located between 4° N and 34° S. In: A.R. ROBINSON, K.H. BRINK, eds. The sea. New York: Wiley. pp. 209-251.; Campos et al., 2000Campos, E.J.D., Velhote, D. and da Silveira, I.C.A., 2000. Shelf break upwelling driven by Brazil Current cyclonic meanders. Geophysical Research Letters, vol. 27, no. 6, pp. 751-754. http://dx.doi.org/10.1029/1999GL010502.
http://dx.doi.org/10.1029/1999GL010502...
). The combination of these factors leads to intrusion of cold and nitrate-rich waters from the SACW into the coast (Acha et al., 2004Acha, E.M., Mianzan, H.W., Guerrero, R.A., Favero, M. and Bava, J., 2004. Marine fronts at the continental shelves of austral South America physical and ecological processes. Journal of Marine Systems, vol. 44, no. 1-2, pp. 83-105. http://dx.doi.org/10.1016/j.jmarsys.2003.09.005.
http://dx.doi.org/10.1016/j.jmarsys.2003...
) altering the physical conditions and also enhancing water nutrient concentrations (Valentin, 1984VALENTIN, J.L., 1984. Analyses des parameters hydrobiologiques danslaremontée de Cabo Frio (Brésil). Marine Biology, vol. 82, pp. 259-276.). Consequently, the primary productivity of Brazilian Southeast increases, particularly in Cabo Frio, Rio de Janeiro State (23°S) (De Léo and Pires-Vanin, 2006De Leo, F.C. and Pires-Vanin, A.M.S., 2006. Benthic megafauna communities under the influence of the South Atlantic Central Water intrusion onto the Brazilian SE shelf: a comparison between an upwelling and a non-upwelling ecosystem. Journal of Marine Systems, vol. 60, no. 3-4, pp. 268-284. http://dx.doi.org/10.1016/j.jmarsys.2006.02.002.
http://dx.doi.org/10.1016/j.jmarsys.2006...
).

Sampling was carried out in six stations (5, 10, 15, 25, 35, and 45m depth) parallel to the coast line (Figure 1). The shallowest stations were categorized in this study as the “Inner Area” (5, 10 and 15m depth), whereas the deepest ones were categorized as “Outer Area” (25, 35 and 45m depth). A shrimp fishing boat equipped with an otter-trawl net with an opening of 4.5m, 200mm mesh size and15mm in the cod end was used. The stations were trawled over a 15 minutes period at a constant speed of 2.0 knot through a 1km stretch. In the laboratory, shrimp were identified following Pérez Farfante and Kensley (1997)Pérez-Farfante, I. and Kensley, B., 1997. Penaeoid and Segestoid shrimps and prawns of the World. Keys and diagnosese for the families and genera. Paris: Museum National d'Histoire Naturelle, 233 p. Memoires du Museum National d'Histoire Naturel. and Costa et al. (2003)COSTA, R.C., FRANSOZO, A., MELO, G.A.S. and FREIRE, F.A.M., 2003. An illustrated key for Dendrobranchiata shrimps from the northern coast of São Paulo state, Brazil. Biota Neotropica, vol. 3, no. 1, pp. 1-12..The total wet weight (in grams) was obtained for each species in each trawl. A 300g sub-sample was randomly selected and all the individuals were counted and examined according to sex and length. Thus, based on the subsample and the total biomass, the estimate of the total number of individuals of each species in each station was determined. When the catch did not exceed 300g, all shrimps were measured (lowest sample size was 01 individual).

Figure 1
Study area evidencing the upwelling region and the sampling area. Location of stations (5-45 m of depth) and major ocean currents of the South Atlantic. ACC: Antarctic Circumpolar Current, MC: Malvinas Current, SAC: South Atlantic Current, SEC: South Equatorial Current, BC: Brazilian Current (Modified from Peterson and Stramma, 1991PETERSON, R. and STRAMMA, L., 1991. Upper-level circulation in the South Atlantic Ocean. Progress in Oceanography, vol. 26, no. 1, pp. 1-73.).

Salinity and temperature (°C) were measured monthly in the surface and near the bottom in each station using a Van Dorn bottle. In the laboratory, salinity was verified with a manual salinometer calibrated with distilled water. Water temperature was verified with a mercury thermometer immediately after sampling in a thermic isolated container in the shade. Depth was determined using an echobathymeter coupled with a Global Positioning System (GPS). Sediment samples were also collected in each season of the year in all sampling station using a Van Veen grab (0.06 m2).Details of the methods used to measure those parameters are described by Negreiros-Fransozo et al. (1991)NEGREIROS-FRANSOZO, M.L., FRANSOZO, A., PINHEIRO, M.A.A., MANTELATTO, F.L. and SANTOS, S., 1991. Caracterização física e química da enseada da Fortaleza, Ubatuba, SP. Revista Brasileira de Geografia, vol. 21, no. 2, pp. 114-120..

The periods under upwelling influence were identified through the Temperature-Salinity diagram (T-S) and by monthly difference between the highest surface temperature and the lowest bottom temperature.

Shrimp abundance (dependent variable) was compared temporally between years (years I: March 2008 to February 2009; year II: March 2009 to February 2010) and seasons (independent variables): autumn (March-May), winter (June-August), spring (September-November) and summer (December-February) using an analysis of variance (nested ANOVA) (α 5%) model, with seasons nested within years; it was also compared spatially between the station(independent variables) using an analysis of variance (one-way ANOVA) (α 5%) model. A post-hoc Tukey test was used to assess differences between stations.Normality of the data was examined by Levene’s test.

The relationship between abiotic factors (salinity, temperature, phi and organic matter content) and the abundance of individuals was assessed with Multiple Linear Regression analysis at the 5% significance level. For selecting the best model to represent the abundance of individuals in relation to the abiotic variables were generated models with all combinations of environmental variables that the number of shrimp is a constant. These models were compared using the Akaike Information Criterion (AIC). The best model was the one with the lowest AIC, which combines increased verisimilitude and parsimony (Sakamoto et al, 1986Sakamoto, Y., Ishiguro, M. and Kitagawa, G., 1986. Akaike information criterion statistics. Tokio: KTK Scientific Publisher/D. Riedel, 290 p.). According to Burnham and Anderson (2004)Burnham, K.P. and ANDERSON, D.R., 2004. Multimo delinference: Understanding AIC e BIC in model. Sociological Methods Reseach, vol. 33, no. 2, pp. 261-304., models with differences in AIC <2 do not show a statistically significant difference. Analyzes were performed with R software (version 3.1.2) using Vegan package (Oksanen et al., 2011OKSANEN, J., BLANCHETT, F.G., KINDT, R., LEGENDRE, P., MINCHIN, P.R., O’HARA, R.B., SIMPSON, G.L., SOLYMOS, P., STEVENS, M.H.M. and WAGNER, H.2011Vegan: community Ecology Package. R Package 2.0.3softwareR-Forge).The data were transformed by natural logarithm for the purpose of satisfying analytic premises (Zar, 1996ZAR, J.H., 1996. Biostatistical analysis. Upper Saddle River: Prentice Hall. 662 p.).

3 Results

During the study period the water masses Coastal Water (CW), Tropical Water (TW) and South Atlantic Central Water (SACW) were identified. It was evident the influence of SACW during spring-summer months in both years, and in autumn (March-April) of the second year (Figure 2).

Figure 2
T-S Diagram showing the temporal variation of water temperature and salinity during the sampling period at upwelling area studied, Southeastern coast of Brazil. CW: Coastal Water; TW: Tropical Water; SACW: South Atlantic Central Water. (Autumn: March-May; Winter June-August; Spring September-November; and Summer means December-February).

The smallest mean value of bottom salinity was recorded during March/2009, mainly in Inner Area (27.0±1.00), when it was compared to Outer Area (31.7±3.21). Contrarily, the greater values were verified in December/2008 (38.8±0.12) and October/2009 (37.0±1.00) in Inner Area, and April/2009 and Mach/2008 (37.7±0.58 e 37.3±0.58) in Outer Area (Figure 3).

Figure 3
Average, maximum and minimum salinity values for each month in “Inner Area” (5, 10 and 15 m) and “Outer Area” (25, 35 and 45 m), sampled from March 2008 to February 2010.

The smaller mean values of bottom temperature were observed in spring and summer of both years, mainly in January/2010 and November/2009 in Inner and Outer Area, respectively. The opposite was observed in winter with greater mean bottom temperature values (Figure 4).

Figure 4
Average, maximum and minimum temperature (°C) values for each month in “Inner Area” (5, 10 and 15 m) and “Outer Area” (25, 35 and 45 m) sampled from March 2008 to February 2010.

The sediment in the Inner Area was composed mainly of medium sand and fine sand (phi varied from 1.23 (±0.5) to 2.79 (±1.6)), and a low percentage of organic matter. In Outer Area the sediment was composed mainly of silt and clay (mean values above 5.49) and a greater content of organic matter (Figure 5).

Figure 5
Granulometric Classes (%) and Organic Matter Content of the sediment for each transect sampled from March 2008 to February 2010.

A total of 7146 individuals were collected during the present study. About96% of all shrimps were caught in the shallow area, i.e., depths <20m (Figure 6). The highest shrimp abundances occurred during winter and spring. Conversely, lowest abundance occurred during summer and autumn, particularly during summer 2009.The analysis of variance (nested ANOVA) indicates no significant difference in temporal comparison abundance between seasons (F=0.96; p=0.45) but it was marginally significant between years (F=3.32; p=0.07).The analysis of variance (one-way ANOVA) indicates significant difference in spatial comparison abundance between stations (F=35.0; p=0.00) (Table 1).

Figure 6
Average, maximum and minimum number of individual for each station sampled from March 2008 to February 2010.
Table 1
Number of individuals in each month and station sampled from March 2008 to February 2010, indicating the results of the Tukey test.

The multiple regression analysis performed using the selected environmental variables (salinity, temperature, organic matter content and phi) and the abundance of Xiphopenaeus kroyeri (r2=0.4, p<0.001, F=1.2E-15, n= 144) can be expressed by the following relationship: A = – 15.4 + 7.1t + 4.8s – 1.4om; where: A= abundance; t= bottom temperature (partial correlation = 4.6,r2=0.2, p<0.001); s = bottom salinity (partial correlation =2.3, r2=0.02, p<0.05), om= organic matter content (partial correlation= –2.5,r2=0.3, p<0.05). The abiotic factors temperature and salinity were positively correlated with the number of collected individuals, nonetheless organic matter content was negative correlation. No significant relationship was observed between sediment (phi) and abundance (p> 0.05). The variable depth was not included in this analysis, considering that abiotic variables temperature and salinity are heavily related to the depth, the use of this variable trend analysis results.

4 Discussion

The distribution of X. kroyeri in the study area is intimately associated with the seasonality of the thermal front of SACW. This close association was also observed by Pires-Vanin et al. (2013)Pires Vanin, A.M.S., Arasaki, E. and Muniz, P., 2013. Spatial pattern of benthic macrofauna in a sub-tropical shelf, São Sebastião Channel, southeastern Brazil. Latin American Journal of Aquatic Research, vol. 41, no. 1, pp. 42-56. http://dx.doi.org/10.3856/vol41-issue1-fulltext-3.
http://dx.doi.org/10.3856/vol41-issue1-f...
, on the north coast of São Paulo, where the seasonality of SACW affected macrofauna benthic invertebrates distribution patterns. Furthermore, Dall et al. (1990)Dall, W., HILL, B.J., ROTHLISBERG, P.C. and SHARPLES, D.J., 1990. The biology of the Penaeidae. Advances in Marine Biology, vol. 27, pp. 1-489. and Costa and Fransozo (2004)Costa, R.C. and Fransozo, A., 2004. Abundance and ecologic distribution of the shrimp . Rimapenaeus constrictus (Crustacea: Penaeidae) in the northern coast of São Paulo State, BrazilJournal of Natural History, vol. 38, no. 7, pp. 901-912. http://dx.doi.org/10.1080/0022293021000046441.
http://dx.doi.org/10.1080/00222930210000...
stated that temperature is a major determinant parameter in the temporal distribution of organisms, especially for penaeid shrimp.

The intrusion of SACW in the spring and summer which promoted decrease in the values of bottom temperature especially in deeper areas, allowing individuals to occupy shallower areas, where temperatures remained higher average (> 22 °C). In contrast, the absence of this water mass during the fall and winter provided a rise in the bottom water temperature and consequently an increase in the abundance of X. kroyeri, especially in transects positioned in deeper areas. In the study by Nakagaki and Negreiros-Fransozo (1998)Nakagaki, J.M. and NEGREIROS-FRANSOZO, M.L., 1998. Population biology of (Heller, 1862) (Decapoda: Penaeidae) from Ubatuba bay, São Paulo, Brazil. Xiphopenaeus kroyeriJournal of Shellfish Research, vol. 17, no. 4, pp. 931-935. was also observed variations in the abundance of this species due to greater penetration of SACW in regions closer to the coast. Similar results were observed by Fransozo et al. (2002)Fransozo, A., COSTA, R.C., MANTELATTO, F.L.M., PINHEIRO, M.A.A. and SANTOS, S., 2002. Composition and abundance of shrimp species (Peneidea and Caridea) in Fortaleza bay, Ubatuba, São Paulo, Brazil. In: E. ESCOBAR-BRIONES and F. ALVAREZ, eds. Modern approaches to the study of crustacea. Dordrecht: Kluwer Academic Publishers, pp. 117-125. and Costa et al. (2007)COSTA, R.C., FRANSOZO, A., FREIRE, F.A.M. and CASTILHO, A.L., 2007. Abundance and ecological distribution of the “sete-barbas” shrimp Xipohpenaeuskroyeri(Heller, 1862) (Decapoda: Penaeoidea) in three bays of the Ubatuba region, South-eastern Brazil. Gulf and Caribbean Research, vol. 19, pp. 33-41. for X. kroyeri, everyone conducted in Ubatuba, northern coast of São Paulo state.

Several authors have suggested that penaeoid shrimp distribution is strongly modulated by the texture and organic content of the substrate (Rulifson, 1981RULIFSON, R.A., 1981. Substrate preference of juvenile penaeid shrimp in estuarine habitats. Contributions in Marine Science, vol. 24, pp. 33-52.; Dall et al., 1990Dall, W., HILL, B.J., ROTHLISBERG, P.C. and SHARPLES, D.J., 1990. The biology of the Penaeidae. Advances in Marine Biology, vol. 27, pp. 1-489.; Sanchez, 1997Sánchez, A.J., 1997. Habitat preference of Burkenroad (Crustacea: Decapoda) in a tropical coastal lagoon, southwest Gulf of Mexico. Penaeus duorarumJournal of Experimental Marine Biology and Ecology, vol. 217, no. 1, pp. 107-117. http://dx.doi.org/10.1016/S0022-0981(97)00049-X.
http://dx.doi.org/10.1016/S0022-0981(97)...
; Costa et al. 2007COSTA, R.C., FRANSOZO, A., FREIRE, F.A.M. and CASTILHO, A.L., 2007. Abundance and ecological distribution of the “sete-barbas” shrimp Xipohpenaeuskroyeri(Heller, 1862) (Decapoda: Penaeoidea) in three bays of the Ubatuba region, South-eastern Brazil. Gulf and Caribbean Research, vol. 19, pp. 33-41.). Our results contradict these assertions since no correlation was found between X. kroyeri and texture of the sediment, and a negative correlation was observed between their abundance and organic matter content of the substrate. A possible hypothesis is that this result is a reflection of the high catch of X. kroyeri in the shallower areas where the organic matter content is low; this shrimp species occurs at temperatures above 21°C (Costa et al., 2007COSTA, R.C., FRANSOZO, A., FREIRE, F.A.M. and CASTILHO, A.L., 2007. Abundance and ecological distribution of the “sete-barbas” shrimp Xipohpenaeuskroyeri(Heller, 1862) (Decapoda: Penaeoidea) in three bays of the Ubatuba region, South-eastern Brazil. Gulf and Caribbean Research, vol. 19, pp. 33-41.) and in the present study area, stations with predominantly muddy sediments showed lower temperature than 21°C.This leads to assume that the temperature in these areas is the primary factor in the establishment of individuals of this species.

The sediment in shallow areas was predominantly medium and fine sand and, conversely, the outer area was characterized by sediment composed of silt and clay. Garcêz (2007)GARCÊZ, D.S., 2007. Caracterização da pesca artesanal autônoma em distintos compartimentos fisiográficos e suas áreas de influência, no estado do Rio de Janeiro. Rio de Janeiro: Universidade Federal do Rio de Janeiro, 125 p. PhD Thesis in Geography. explained this by the formation of a tombolo submarine (submerged sandy track) between the beach and the Archipelago de Santana included in the study area. This sandy strip provides in shallow areas a removal of fine sediments by wave action, establishing an irregular facies pattern of medium and very coarse sand. The muddy sediments occur preferentially above 15 meters depht. This result also supports the conclusion that the species has a great plasticity in relation to sediment type. Other studies such as those developed in Ubatuba, São Paulo State (Freire et al., 2011FREIRE, F.A.M., LUCHIARI, A.C. and FRANSOZO, V., 2011. Environmental substrate selection and daily habitual activity in shrimp (Heller, 1862) (Crustacea: Penaeioidea). Xiphopeneus kroyeriIndian Journal of Geo-marine Science, vol. 40, no. 3, pp. 325-330.; Costa et al., 2007COSTA, R.C., FRANSOZO, A., FREIRE, F.A.M. and CASTILHO, A.L., 2007. Abundance and ecological distribution of the “sete-barbas” shrimp Xipohpenaeuskroyeri(Heller, 1862) (Decapoda: Penaeoidea) in three bays of the Ubatuba region, South-eastern Brazil. Gulf and Caribbean Research, vol. 19, pp. 33-41.) found that this species prefers muddy sediments, which in this study area occurred in shallower portions.

According to the study results, the temperature is the main factor modeler of abundance and spatial-temporal distribution of X. Kroyeri, being controlled by the variations in temperature caused by the SACW intrusion in the region. Thus, in periods that occurs most influences of the cold waters of SACW in the coast of Macaé, shrimps migrate to shallower depths where the temperature remains higher means. Likewise, the abundance of X. kroyeri suffer temporal variations, being modulated by the higher or lower SACW influence.

Acknowledgments

The authors are grateful to the “Financiadora de Estudos e Projetos (Finep/Ministério de Ciência e Tecnologia) for the financial support to the field work; to the “Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (APQ - 305919/2014-8 and APQ - 406006/2012-1RCC)”, to the “Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ)”, and to the “Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (#09/54672-4 and 010/50188-8-RCC)” for funding; and also to the “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)” for the fellwoship to the first author. We also thank to the “Universidade Federal do Rio de Janeiro (NUPEM/UFRJ)” for the infrastructure provided for the execution of this project and our collaborators (NEBECC and LABCAM members) for field and laboratory assistance. All samplings were carried out in accordance with Brazilian state and federal laws (Instituto Chico Mendes de Biodiversidade/ICMBio n° 11274).

  • (With 6 figures)

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Publication Dates

  • Publication in this collection
    19 Apr 2016
  • Date of issue
    Jul-Sep 2016

History

  • Received
    24 Mar 2015
  • Accepted
    10 June 2015
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
E-mail: bjb@bjb.com.br