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Distribution pattern of juveniles of the pink shrimps Farfantepenaeus brasiliensis (Latreille, 1817) and F. paulensis (Pérez-Farfante, 1967) on the southeastern Brazilian coast

Abstract

The spatio-temporal distribution of juveniles of the pink shrimps Farfantepenaeus brasiliensis (Latreille, 1817) and Farfantepenaeus paulensis (Pérez-Farfante, 1967) in the Ubatuba region (SP) was investigated. Sampling was performed in the bays of Ubatumirim (UBM), Ubatuba (UBA) and Mar Virado (MV). A total of 2,018 F. brasiliensis and F. paulensis were collected. The largest catch of juveniles of both species occurred in UBA (N = 867), followed by UBM (N = 729) and MV (N= 422). The bottom sediment in MV had the highest silt and clay content, which explains the negative correlation of the substrate with the abundance of both species. Temperature was positively correlated with the abundance of both species. Juveniles were highly abundant in shallower areas in the summer of 1998. The high rainfall in this El Niño period may have lowered the salinity in estuarine waters and led the shrimps to move to coastal areas in search of higher salinities such as in bays. With this unusually early reduction in salinity, individuals migrated to the bay before the closed season began and thus became more exposed to fishing. We confirmed that monitoring environmental variations, especially in El Niño years, is essential for understanding the distribution patterns of juveniles of both species.

Key words
Abundance; Penaeidae; El Niño; closed season

Introduction

The pink shrimps Farfantepenaeus brasiliensis (Latreille, 1817) and Farfantepenaeus paulensis (Pérez-Farfante, 1967) are among the most important penaeids commercially exploited in the southeastern Brazilian coast (Valentini et al., 1991Valentini, H.; D'Incao, F.; Rodrigues, F.L.; Neto, J.E.R. and Rahn, E. 1991. Análise da pesca do camarão-rosa, Penaeus brasiliensis e Penaeus paulensis, nas regiões Sudeste e Sul do Brasil. Atlântica , 13(1): 143-157.; 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. Atlântica , 24(2): 103-116.; Dias-Neto, 2011Dias-Neto, J. 2011. Proposta de Plano Nacional de Gestão para o uso Sustentável de Camarões Marinhos do Brasil. Brasília, IBAMA, 242p.). The sharp decrease in pink shrimps catches along the Brazilian coast, especially in the southeastern and southern regions, seems to indicate that the fishing effort is dangerously high (Dias-Neto, 1991Dias-Neto, J. 1991. Pesca dos camarões na costa norte do Brasil. Atlântica , 13(1): 21-28.; Dias-Neto and Dornelles, 1996Dias-Neto, J. and Dornelles, L.D.C. 1996. Diagnóstico da Pesca Marítima do Brasil. Brasília, IBAMA/MMA, 163p.; Santos et al., 2008Santos, J.L; Severino-Rodrigues, E. and Vaz-Dos-Santos, A.M. 2008. Estrutura populacional do camarão-branco Litopenaeus schmitti nas regiões estuarina e marinha da Baixada Santista, São Paulo, Brasil. Boletim do Instituto da Pesca, 34(3): 375-389.). During the 1970s, the harvested biomass averaged over 16,000 t y-1, but it declined to < 500 t y-1 in the late 1980s and 1990s (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. Atlântica , 24(2): 103-116.). Although species of this genus are not included in the Red List of endangered animals of the International Union for Conservation of Nature (IUCN), the Chico Mendes Institute for Biodiversity Conservation (ICM-Bio) classifies Farfantepenaeus Burukovsky, 1997 species as having "insufficient data", which means that these species have a priority for evaluations of conservation status (Brasil, 2014Brasil. Ministério do Meio Ambiente 2014. Portaria No 43, de 31 de Janeiro de 2014. Institui o Programa Nacional de Conservação das Espécies Ameaçadas de Extinção.). Additionally, no specific information is available on the fishing effort for each species, which precludes a more accurate diagnosis (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. Atlântica , 24(2): 103-116.; Santos et al., 2008Santos, J.L; Severino-Rodrigues, E. and Vaz-Dos-Santos, A.M. 2008. Estrutura populacional do camarão-branco Litopenaeus schmitti nas regiões estuarina e marinha da Baixada Santista, São Paulo, Brasil. Boletim do Instituto da Pesca, 34(3): 375-389.).

Species of Farfantepenaeus have a Type II life cycle, which includes spawning in offshore areas and postlarvae migrating to estuarine regions and remaining there until the juvenile stage is completed (Dall et al., 1990Dall, W.; Hill, B.J.; Rothlisberg, P.C. and Sharples, D.J. 1990. The biology of the Penaeidae. In: J.H.S. Blaxter and A.J. Southward (eds), Advances in Marine Biology, 27: 1-489. Academic Press, London.; Costa et al., 2008Costa, R.C.; Lopes, M.; Castilho, A.L.; Fransozo, A. and Simões, S.M. 2008. Abundance and distribution of juvenile pink shrimps Farfantepenaeus spp. in a mangrove estuary and adjacent bay on the northern shore of São Paulo State, southeastern Brazil. Invertebrate Reproduction and Development, 52(1-2): 51-58.). After 2-4 months, juveniles migrate down the estuary and pass through the coastal region, moving toward oceanic waters and completing their life cycle (Benfield and Downer, 2001Benfield, M.C. and Downer, R.G. 2001. Spatial and temporal variability in the near shore distributions of post larval Farfantepenaeus aztecus along Galveston Island, Texas. Estuarine, Coastal and Shelf Science, 52(4): 445-456.; Pérez-Castañeda and Defeo, 2001Pérez-Castañeda, R. and Defeo, O. 2001. Population variability of four sympatric penaeid shrimps (Farfantepenaeus spp.) in a tropical coastal Lagoon of Mexico. Estuarine, Coastal and Shelf Science, 52(5): 631-641.). If juveniles migrate in months outside the closed season period, they will be caught in large numbers in the coastal region by artisanal fisheries targeting the seabob shrimp Xiphopenaeus kroyeri (Heller, 1862), especially on the southern and southeastern Brazilian coast (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 Xiphopenaeus kroyeri (Heller, 1862) (Decapoda: Penaeoidea) in three bays of the Ubatuba region, Southeastern, Brazil. Gulf and Caribbean Research, 19: 33-41.). As these individuals have not yet reproduced, such captures may have serious effects on the maintenance of Farfantepenaeus populations.

The distribution of juveniles of Farfantepenaeus is mainly related to salinity. Most individuals of F. brasiliensis are caught at 15-30 (Branco and Verani, 1998aBranco, J.O. and Verani, J.R. 1998. Aspectos bioecológicos do camarão-rosa Penaeus brasiliensis Latreille (Natantia, Penaeidae) da lagoa da Conceição, Florianópolis, Santa Catarina, Brasil. Revista brasileira de Zoologia, 15(2): 345-351.; 1998bBranco, J.O. and Verani, J.R. 1998. Aspectos bioecológicos do camarão-rosa Penaeus brasiliensis Latreille (Natantia, Penaeidae) da lagoa da Conceição, Florianópolis, Santa Catarina, Brasil. Revista brasileira de Zoologia, 15(2): 345-351.), whereas F. paulensis is more often caught at lower salinities, primarily below 20 (D'Incao, 1991D'Incao, F. 1991. Pesca e biologia de Penaeus paulensis na Lagoa dos Patos. Atlântica, 13(1): 159-169.). Regarding the other variables, penaeid juveniles also prefer finer sediments with higher organic-matter content (Dall et al., 1990Dall, W.; Hill, B.J.; Rothlisberg, P.C. and Sharples, D.J. 1990. The biology of the Penaeidae. In: J.H.S. Blaxter and A.J. Southward (eds), Advances in Marine Biology, 27: 1-489. Academic Press, London.) and high temperatures (Costa et al., 2008Costa, R.C.; Lopes, M.; Castilho, A.L.; Fransozo, A. and Simões, S.M. 2008. Abundance and distribution of juvenile pink shrimps Farfantepenaeus spp. in a mangrove estuary and adjacent bay on the northern shore of São Paulo State, southeastern Brazil. Invertebrate Reproduction and Development, 52(1-2): 51-58.).

Recent studies have shown that rainfall plays an important role in the distribution of juveniles on Brazilian coast, as it alters mainly the salinity (Santos et al., 2008Santos, J.L; Severino-Rodrigues, E. and Vaz-Dos-Santos, A.M. 2008. Estrutura populacional do camarão-branco Litopenaeus schmitti nas regiões estuarina e marinha da Baixada Santista, São Paulo, Brasil. Boletim do Instituto da Pesca, 34(3): 375-389.; Bochini et al., 2014Bochini, G.L.; Fransozo, A.; Castilho, A.L.; Hirose, G.L. and Costa, R.C. 2014. Temporal and spatial distribution of the commercial shrimp Litopenaeus schmitti (Burkenroad, 1936) (Dendrobranchiata: Penaeidae) in the southeastern Brazilian coast. Journal of the Marine Biological Association of the United Kingdom, 94(5): 1001-1008.). Also, the El Niño phenomenon, which occurs on inter-annual scales, is the main source of short-term climate variability and can intensify rainfall in southern and southeastern Brazil (Silva, 2000Silva, J.F. 2000. El Niño, o fenômeno climático do século. Brasília, Editora Thesaurus, 139p. ). Bochini et al. (2014)Bochini, G.L.; Fransozo, A.; Castilho, A.L.; Hirose, G.L. and Costa, R.C. 2014. Temporal and spatial distribution of the commercial shrimp Litopenaeus schmitti (Burkenroad, 1936) (Dendrobranchiata: Penaeidae) in the southeastern Brazilian coast. Journal of the Marine Biological Association of the United Kingdom, 94(5): 1001-1008. recorded earlier juvenile migration of Litopenaeus schmitti (Burkenroad, 1936) in years when El Niño was more intense.

Studies of the distribution pattern of a species are essential to develop applicable and effective management measures, especially considering the high commercial value of species of Farfantepenaeus. This study investigated the temporal and spatial variation in the catch of juveniles of F. brasiliensis and F. paulensis in three bays at Ubatuba (Ubatumirim, Ubatuba and Mar Virado), São Paulo, Brazil. We also studied the relationship between environmental parameters (temperature, salinity, rainfall, and sediment organic-matter content and granulometry) and the distributions of these species. Additionally, considering that the closed season period in southern and southeastern Brazil extends from March to May, we evaluated whether the closed season is effective in protecting the two species in the study region.

Material and Methods

Shrimp sampling

Shrimp were collected monthly from January 1998 to December 1999, in the bays of Ubatumirim (UBM) (23°20'15.7338"S 044°53'39.2136"W), Ubatuba (UBA) (23°27'00.0"S 045°03'18.0"W) and Mar Virado (MV) (23°31'43.6548"S 045°12'54.849"W), located in the Ubatuba region, northern coast of São Paulo. In each bay, six stations were sampled monthly at depths up to 20 m. Four stations were located at mean depths of 5 (IV), 10 (III), 15 (II) and 20 m (I); and the other two were adjacent to rocky shores (an exposed and a sheltered shore, stations V at 9 m and VI at 6.5 m, respectively) (Fig. 1).

Figure 1
Map of Ubatuba on the coast of São Paulo, showing the three bays and their respective sampling stations.

A shrimp-fishing boat equipped with double-rig nets (mesh size 20 mm and 18 mm in the cod end) was used for trawling. Each trawl was performed over a 30-min period, covering a total area of 18,000 m2.

Environmental factors

The salinity and temperature of the bottom water, and the organic-matter content (%) and granulometry (φ) of the sediment were obtained at each sampling station. A Nansen bottle was used for bottom-water samples. Salinity was measured with an optical refractometer and temperature (°C) with a mercury thermometer (0.1°C accuracy). An echo sounder coupled to a GPS (Global Positioning System) was used to provide the depth (m) of each sampling station. The rainfall data were obtained in http://www.ciiagro.org.br.

The values ​​of sediment organic-matter content and granulometry were obtained from samples collected seasonally with a Van Veen grab (area of 0.06 m2) and frozen until the analysis. Detailed descriptions of the methods used to determine the granulometric composition and the organic-matter percentage of the sediment can be found in 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 Xiphopenaeus kroyeri (Heller, 1862) (Decapoda: Penaeoidea) in three bays of the Ubatuba region, Southeastern, Brazil. Gulf and Caribbean Research, 19: 33-41. and Bochini et al. (2014)Bochini, G.L.; Fransozo, A.; Castilho, A.L.; Hirose, G.L. and Costa, R.C. 2014. Temporal and spatial distribution of the commercial shrimp Litopenaeus schmitti (Burkenroad, 1936) (Dendrobranchiata: Penaeidae) in the southeastern Brazilian coast. Journal of the Marine Biological Association of the United Kingdom, 94(5): 1001-1008..

Data analysis

Tests for homoscedasticity (Levene tests) and normality (Shapiro-Wilk tests) were first performed as prerequisites for the statistical test, using an Excel(r) spreadsheet divided into rows and columns. When necessary, data were transformed with Box-Cox transformation, using the statistical software PAST - PAleontological STatistics - Version 3.02) power transformation in order to select the most appropriate procedure (Sokal and Rohlf, 1995Sokal, R.R. and Rohlf, F.J. 1995. Biometry. New York, W.H. Freeman and Company, 887p.). All data sets were normally distributed, with homogeneous variances.

Shrimp abundance (dependent variable) was compared temporally between years and among seasons (independent variables): summer (January-March), autumn (April-June), winter (July-September) and spring (October-December). Abundance was also compared spatially among bays and collection stations (independent variables) using an analysis of variance model (nested ANOVA, α = 5%) (Statistica 7.0 program), with stations nested within area and seasons nested within years. A post-hoc Tukey test was used to assess differences among seasons, bays and stations.

A redundancy analysis (RDA) (R-project program) was used to assess the amount of variation in faunal densities related to a set of habitat environmental characteristics (Ter Braak, 1996Ter Braak, C.J.F. 1996. Unimodal Models to Relate Species to Environment. Wageningen, DLO-Agricultural Mathematics Group, 266p.). Previous analysis of the main species showed a linear response in their abundance in relation to the environmental variables used. The use of RDA provides a larger percentage of the variance explained regarding the canonical correspondence analysis (CCA), which is more suitable when there is a unimodal response. The set of environmental variables used in RDA calculations comprised the bottom salinity and bottom temperature, organic-matter content (%) and grain size of sediments (φ) and rainfall.

Results

Environmental factors

The mean values of bottom-water salinity were similar in the two years sampled, with 34.23 ± 1.43 in 1998 and 34.08 ± 1.34 in 1999. The highest salinity values (> 35) were found during summer and autumn in 1998 and autumn in 1999. The lowest salinity values occurred during early spring (September and October) in 1998 and during winter and spring (except November) in 1999 (Fig. 2). Spatially, despite the lower values recorded at shallower stations and the higher values recorded at deeper stations, the mean salinity did not vary significantly among sampling stations (Fig. 3).

Figure 2
Mean values (minimum and maximum) of salinity and temperature (°C) of the bottom water from January 1998 to December 1999, in each season (Su = summer, Au = autumn, Wi = winter, Sp = spring), in the bays of Ubatumirim (UBM), Ubatuba (UBA) and Mar Virado (MV).

Figure 3
Mean values (minimum and maximum) of salinity and temperature (°C) of bottom water sampled from January 1998 to December 1999, at each sampling station, in the bays of Ubatumirim (UBM), Ubatuba (UBA) and Mar Virado (MV).

The mean values of bottom-water temperature were higher in the first year of sampling in all three bays. The highest mean temperature occurred in the summer of both years and at shallower stations, while lower values ​​were observed in winter 1998 and spring of 1999 and at deeper stations (Figs. 2, 3).

Differences in mean organic-matter content levels were found among the bays, with the deeper stations, located close to the bay mouth (I and II), showing the lowest levels (Tab. 1).

Table 1.
Mean values of sediment parameters (φ and % OM) sampled from January 1998 to December 1999, at each sampling station, in the bays of Ubatumirim, Ubatuba and Mar Virado.

The amount of mud (φ > 4) in the sediments decreased northward, i.e., from MV to UBM (Tab. 1). In MV, the silt+clay fraction (φ > 4) predominated at almost all stations. A predominance of fine and very fine sand, associated with silt and clay, was observed in Ubatuba, particularly in UBM, except for stations I and VI in UBA and station I in UBM (Tab. 1).

The mean rainfall was higher during the first year of sampling (249.44 ± 168.20 mm). In the second year, the mean was 195.49 ± 101.64 mm. Rainfall was most intense during spring and summer of both years (Fig. 4).

Figure 4.
Cumulative values for monthly rainfall (mm) and number of individuals of Farfantepenaeus brasiliensis and F. paulensis sampled from January 1998 to December 1999 at Ubatuba, São Paulo.

Abundance and distribution

In total, 2,018 juveniles were collected during the study period, with 1,380 individuals of F. brasiliensis (900 in 1998 and 480 in 1999) and 638 of F. paulensis (422 in 1998 and 216 in 1999). There was no statistically significant difference between the abundance and the sampled years, but there were differences between abundance and seasons (Tab. 2), with larger catches recorded in summer and autumn (Fig. 5). In 1998, the highest abundance was observed in summer, while in 1999 the highest abundance occurred in autumn, especially for F. brasiliensis. Over 50% of F. brasiliensis individuals sampled in 1999 were captured in April (Figs. 4, 5).

Figure 5.
Number of individuals of Farfantepenaeus brasiliensis and F. paulensis captured seasonally from January 1998 to December 1999 in the bays of Ubatumirim (UBM), Ubatuba (UBA) and Mar Virado (MV).

Table 2.
Results of nested ANOVA for the number of individuals (log + 1 transformed) of Farfantepenaeus brasiliensis and F. paulensis collected in three bays of the Ubatuba region, from January 1998 to December 1999.

Spatially, the highest abundance of juveniles occurred in UBA, with 867 individuals captured (562 of F. brasiliensis and 305 of F. paulensis), followed by UBM, with 729 individuals (509 F. brasiliensis and 220 F. paulensis), and MV, with 422 individuals (309 F. brasiliensis and 113 F. paulensis). Only the abundance of F. paulensis differed among bays, where MV differed from UBM (Nested ANOVA, p < 0.01). For both species there were statistically significant differences among the sampling stations (Nested ANOVA, p < 0.01) (Tab. 3), with the highest catch of F. brasiliensis at stations II and VI in UBM, IV and VI in UBA and I and VI in MV; for F. paulensis, the highest catch occurred in V and VI in UBM, IV and VI in UBA and I and VI in MV (Fig. 6). For both species, the highest capture occurred in station VI in the three bays sampled (Fig. 6).

Table 3.
Results of Nested ANOVA for the number of individuals (log + 1 transformed) of Farfantepenaeus brasiliensis and F. paulensis collected from January 1998 to December 1999 in the bays of Ubatumirim, Ubatuba and Mar Virado.

Figure 6.
Number of individuals of Farfantepenaeus brasiliensis and F. paulensis captured at each sampling station in the bays of Ubatumirim (UBM), Ubatuba (UBA) and Mar Virado (MV), from January 1998 to December 1999.

The relationship between abundance and environmental factors

The first and second axes of the redundancy analysis (RDA) represent the relationships between shrimp abundance and environmental factors (Fig. 7A-C). The Monte-Carlo test indicated that these two canonical axes were significant together (p <0.005), but the results are explained by axis 1 in the graph (Tab. 4; Fig. 7A-C).

Figure 7.
Redundancy analysis showing the relative abundance of Farfantepenaeus brasiliensis and F. paulensis with environmental factors sampled from January 1998 to December 1999 in the bays of Ubatumirim (A), Ubatuba (B) and Mar Virado (C).

Table 4.
Redundancy analysis (RDA) of the abundance of Farfantepenaeus brasiliensis and F. paulensi s in relation to environmental variables that best explained the variation of the sampling data in three bays in the Ubatuba region, from January 1998 to December 1999.

Environmental variables correlated differently with the abundance of shrimp found in each bay. The bottom-water temperature was the common variable for the three bays, and correlated positively with the abundance of both species. The highest captures occurred in water temperatures ​​above 21°C (Tab. 4; Fig. 7A-C). Rainfall correlated positively in two of the three bays (Tab. 4). The highest rainfall values were recorded during January and February 1998, when the highest abundances of juveniles were found. In 1999, with the decrease in rainfall, especially in January and February, the greatest abundances of juveniles occurred in April (Fig. 4).

Temperature and rainfall correlated positively with the abundance of both species in UBM (Fig. 7A), while in UBA there was a positive relationship only with temperature (Fig. 7B). In MV, there was a correlation with temperature, rainfall and sediment granulometry (φ) (Fig. 7C). Temperature and rainfall correlated positively with abundance; the largest catches occurred in seasons of higher temperatures and greater precipitation. Granulometry correlated negatively with the number of juveniles; the greatest abundance was observed at the station with the lowest φ value, i.e., with larger-diameter grains (Fig. 7C). However, this sediment is still considered very fine, with a predominance of silt + clay (φ > 4) (Tab. 1).

Discussion

We observed a seasonal temporal distribution of juveniles of F. brasiliensis and F. paulensis, i.e., the shrimp migrated from the estuary to the bay between January and May, partially agreeing with the study of Costa et al. (2008Costa, R.C.; Lopes, M.; Castilho, A.L.; Fransozo, A. and Simões, S.M. 2008. Abundance and distribution of juvenile pink shrimps Farfantepenaeus spp. in a mangrove estuary and adjacent bay on the northern shore of São Paulo State, southeastern Brazil. Invertebrate Reproduction and Development, 52(1-2): 51-58.). These authors recorded the migration to UBA from March to May.

This difference in the months in which juveniles are present is related to rainfall. The high pluviosity in early 1998 was a result of El Niño, which is consequence of the warming waters and heavy rains in southern and southeastern Brazil (Silva, 2000Silva, J.F. 2000. El Niño, o fenômeno climático do século. Brasília, Editora Thesaurus, 139p. ). The El Niño in this period was the strongest in 50 years, which explains the high rainfall values recorded (Glantz, 2001Glantz, M.H. 2001. Currents of Change: Impacts of El Niño and La Niña on Climate and Society. Cambridge, Cambridge University Press, 268p.; Berlato et al., 2007Berlato, M.A.; Martins, E.J.; Cordeiro, A.P.A. and Oderich, E.H. 2007. Tendência observada da precipitação pluvial anual e estacional do estado do Rio Grande do Sul e relação com a temperatura da superfície do mar do Oceano Pacífico. In: XV Congresso Brasileiro de Agrometeorologia, Aracaju, Brazil. ; Filgueira et al., 2007Filgueira, H.J.A.; Neto, A.F.S. and Barbosa, M.P. 2007. Impacto dos eventos ENOS (El Niño-Oscilação Sul) nas precipitações pluviométricas, nos recursos hídricos superficiais e na degradação do solo em região do semi-árido brasileiro. In: Anais XIII Simpósio Brasileiro de Sensoriamento Remoto, Florianópolis, Brasil, INPE, 3893-3898.; Britto et al., 2008Britto, F.P.; Barletta, R. and Mendonça, M. 2008. Variabilidade espacial e temporal da precipitação pluvial no Rio Grande do Sul: Influência do fenômeno El Niño Oscilação Sul. Revista Brasileira de Climatologia, 1: 37-48.; Pereira and D'Incao, 2012Pereira, N. and D'Incao, F. 2012. Precipitação pluvial na bacia hidrográfica da lagoa dos patos, no período de 1964 a 2007 e suas associações com as safras de camarão-rosa. Atlântica , 34(2): 145-156.). In 1999, due to the smaller amount of rain, especially in summer, this migration occurred in later months (in autumn and during the closed season period).

Similar results were found by Bochini et al. (2014Bochini, G.L.; Fransozo, A.; Castilho, A.L.; Hirose, G.L. and Costa, R.C. 2014. Temporal and spatial distribution of the commercial shrimp Litopenaeus schmitti (Burkenroad, 1936) (Dendrobranchiata: Penaeidae) in the southeastern Brazilian coast. Journal of the Marine Biological Association of the United Kingdom, 94(5): 1001-1008.) for the white shrimp L. schmitti. For this species, however, the advance of migration from May to April did not result in the capture of recruits by fishing, as this event coincided with the closed season.

The positive association between rainy periods and penaeid juvenile migration, mainly for those with a type II life cycle, was also reported by Garcia and Le Reste (1981Garcia, S. and Le Reste, L. 1981. Life cycles, dynamics, exploitation and management of coastal penaeid shrimp stocks. FAO Fisheries Technical Paper, 203: 215p. ) and Dall et al. (1990Dall, W.; Hill, B.J.; Rothlisberg, P.C. and Sharples, D.J. 1990. The biology of the Penaeidae. In: J.H.S. Blaxter and A.J. Southward (eds), Advances in Marine Biology, 27: 1-489. Academic Press, London.). The high rainfall volumes markedly lowered the salinity values in estuarine waters. As individuals grow, their osmoregulatory capacity decreases, which leads the juveniles to migrate to more favorable areas such as the shallower waters of the bays (Dall et al., 1990Dall, W.; Hill, B.J.; Rothlisberg, P.C. and Sharples, D.J. 1990. The biology of the Penaeidae. In: J.H.S. Blaxter and A.J. Southward (eds), Advances in Marine Biology, 27: 1-489. Academic Press, London.). This also probably occurred for the species of the present study, as laboratory experiments on postlarvae of F. paulensis showed high mortalities in salinities lower than 3 (Tsuzuki et al., 2003Tsuzuki, M.Y.; Cavalli, R.O. and Bianchini, A. 2003. Effect of salinity on survival, growth, and oxygen consumption of the pink shrimp Farfantepenaeus paulensis (Pérez-Farfante, 1967). Journal of Shellfish Research, 22(2): 555-559.). For F. brasiliensis, the highest mortality rates occurred in salinities lower than 15 (Brito et al., 2000Brito, R.; Chimal, M.E. and Rosas, C. 2000. Effect of salinity in survival, growth, and osmotic capacity of early juveniles of Farfantepenaeus brasiliensis (Decapoda: Penaeidae). Journal of Experimental Marine Biology and Ecology, 244(2): 253-263.).

On the other hand, our results completely agree with those of Costa et al. (2008Costa, R.C.; Lopes, M.; Castilho, A.L.; Fransozo, A. and Simões, S.M. 2008. Abundance and distribution of juvenile pink shrimps Farfantepenaeus spp. in a mangrove estuary and adjacent bay on the northern shore of São Paulo State, southeastern Brazil. Invertebrate Reproduction and Development, 52(1-2): 51-58.) in relation to the positive correlation between abundance and water temperature. Most tropical/subtropical penaeid shrimps prefer higher temperatures, as evidenced by several studies performed with: post-larvae and juveniles of Fenneropenaeus merguiensis (De Man, 1888) in two Australian estuaries (Vance et al., 1998Vance, D.J.; Haywood, M.D.E.; Heales, D.S.; Kenyon, R.A. and Loneragan, N.R. 1998. Seasonal and annual variation in abundance of postlarval and juvenile banana prawns Penaeus merguiensis and environmental variation in two estuaries in tropical northeastern Australia: a six year study. Marine Ecology Progress Series, 163: 21-36.); L. schmitti in marine and estuarine areas of Santos and Ubatuba Bay, respectively (Santos et al., 2008Santos, J.L; Severino-Rodrigues, E. and Vaz-Dos-Santos, A.M. 2008. Estrutura populacional do camarão-branco Litopenaeus schmitti nas regiões estuarina e marinha da Baixada Santista, São Paulo, Brasil. Boletim do Instituto da Pesca, 34(3): 375-389.; Bochini et al., 2014Bochini, G.L.; Fransozo, A.; Castilho, A.L.; Hirose, G.L. and Costa, R.C. 2014. Temporal and spatial distribution of the commercial shrimp Litopenaeus schmitti (Burkenroad, 1936) (Dendrobranchiata: Penaeidae) in the southeastern Brazilian coast. Journal of the Marine Biological Association of the United Kingdom, 94(5): 1001-1008.); species of Farfantepenaeus in the estuary and adjacent bay of Ubatuba (Costa et al., 2008Costa, R.C.; Lopes, M.; Castilho, A.L.; Fransozo, A. and Simões, S.M. 2008. Abundance and distribution of juvenile pink shrimps Farfantepenaeus spp. in a mangrove estuary and adjacent bay on the northern shore of São Paulo State, southeastern Brazil. Invertebrate Reproduction and Development, 52(1-2): 51-58.); and X. kroyeri in Ubatuba Bay (Costa et al., 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. Museo Regionale di Scienze Naturali - Torino, 1, 47-58.).

The temperature is highly important for the distribution of penaeid shrimps. This abiotic factor can significantly affect the metabolism (Dall et al., 1990Dall, W.; Hill, B.J.; Rothlisberg, P.C. and Sharples, D.J. 1990. The biology of the Penaeidae. In: J.H.S. Blaxter and A.J. Southward (eds), Advances in Marine Biology, 27: 1-489. Academic Press, London.), mainly the reproductive behavior of some species, as observed for Rimapenaeus constrictus (Stimpson, 1874) (Costa and Franzoso, 2004Costa, R.C. and Fransozo, A. 2004. Reproductive biology of the shrimp Rimapenaeus constrictus (Crustacea, Decapoda, Penaeidae) in Ubatuba region, SP, Brazil. Journal of Crustacean Biology , 24(2): 274-281.), Artemesia longinaris Spence Bate, 1888 (Castilho et al., 2007Castilho, A.L.; Gavio, M.A.; Costa, R.C.; Boschi, E.E.; Bauer, R.T. and Fransozo, A. 2007. Latitudinal variation in population structure and reproductive pattern of the endemic South American shrimp Artemesia longinaris. Journal of Crustacean Biology, 27(4): 548-552. a; 2007b) and Pleoticus muelleri (Spence Bate, 1888) (Castilho et al., 2008bCastilho, A.L.; Costa, R.C.; Fransozo, A. and Negreiros-Fransozo, M.L. 2008. Reproduction and recruitment of the South American red shrimp, Pleoticus muelleri (Crustacea: Solenoceridae), from the southeastern cost of Brazil. Marine Biology Research, 4(5): 361-368.).

In addition to high temperature, the higher incidence of F. paulensis and F. brasiliensis in UBA and UBM was related to their preference for sediments with larger diameters. Similar results were found by Furlan et al. (2013Furlan, M.; Castilho, A.L.; Fernandes-Góes, L.C.; Fransozo, V.; Bertini, G. and Costa, R.C. 2013. Effect of environmental factors on the abundance of decapod crustaceans from soft bottoms off southeastern Brazil. Anais da Academia Brasileira de Ciências, 85(4): 1345-1356.), whose explanation was based on Williams (1958Williams, A.B. 1958. Substrates as a factor in shrimp distribution. Limnology and Oceanography, 3(3): 283-290.), in which the burying behavior of shrimp is related to their ability to excavate, and to the intrinsic respiratory requirements of each species. Sediment grains with larger diameters are more difficult to move, so individuals require more time and expend more energy to bury in this type of substrate (Ruello, 1973Ruello, N.V. 1973. Burrowing, feeding, and spatial distribution of the school prawn Metapenaeus macleayi (Haswell) in the Hunter River region, Australia. Journal of Experimental Marine Biology and Ecology, 13(3): 189-206.). Pink shrimps, however, buried completely in the sediments with larger diameters, as confirmed by Lopes (2012Lopes, M. 2012. Distribuição e dinâmica populacional dos camarões-rosa, Farfantepenaeus brasiliensis (Latreille, 1817) e F. paulensis (Pérez-Farfante, 1967) e do camarão-branco Litopenaeus schmitti (Burkenroad, 1936) (Decapoda: Dendrobranchiata: Penaeidae) no complexo baía-estuário de Santos - São Vicente, São Paulo, Brasil: subsídios científicos para a averiguação do período ideal de defeso. . Universidade Estadual Paulista - UNESP, Botucatu, Brazil, Ph.D. Thesis. 139p. [Unpublished]) under laboratory conditions. In very fine sediments, particles may enter the gills and thus make breathing more difficult. Therefore, species with a preference for fine sediments possess a mechanism that reverses the exhalant water flow, clearing the gills of smaller particles (Ruello, 1973Ruello, N.V. 1973. Burrowing, feeding, and spatial distribution of the school prawn Metapenaeus macleayi (Haswell) in the Hunter River region, Australia. Journal of Experimental Marine Biology and Ecology, 13(3): 189-206.).

For other penaeids such as X. kroyeri and L. schmitti, also abundant in the region, the largest catches occurred in MV, where the sediment is mostly composed of smaller-diameter grains (silt and clay) (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 Xiphopenaeus kroyeri (Heller, 1862) (Decapoda: Penaeoidea) in three bays of the Ubatuba region, Southeastern, Brazil. Gulf and Caribbean Research, 19: 33-41.; Bochini et al., 2014Bochini, G.L.; Fransozo, A.; Castilho, A.L.; Hirose, G.L. and Costa, R.C. 2014. Temporal and spatial distribution of the commercial shrimp Litopenaeus schmitti (Burkenroad, 1936) (Dendrobranchiata: Penaeidae) in the southeastern Brazilian coast. Journal of the Marine Biological Association of the United Kingdom, 94(5): 1001-1008.). When a species inhabits sediment composed of silt and clay, it does not bury completely, a behavior that facilitates respiration (Freire et al., 2011Freire, F.A.M.; Luchiari, A.C. and Fransozo, V. 2011. Environmental substrate selection and daily habitual activity in Xiphopenaeus kroyeri shrimp (Heller, 1862) (Crustacea: Penaeioidea). Indian Journal of Geo-Marine Science, 40(3): 325-330.).

Both pink shrimps were captured in higher abundance at station VI of the three bays, areas protected from wave action. Protected areas have high organic-carbon content (Ameeri and Cruz, 1998Ameeri, A.A. and Cruz, E.M. 1998. Effect of sand substrate on growth and survival of Penaeus semisulcatus de Haan juveniles. Journal of Aquaculture in the Tropics, 13(4): 239-244.), ensuring good environmental conditions with weaker hydrodynamics and larger amounts of food available. Consequently, these areas require less energy for the shrimp to survive in the environment (D'Incao, 1991D'Incao, F. 1991. Pesca e biologia de Penaeus paulensis na Lagoa dos Patos. Atlântica, 13(1): 159-169.), which can facilitate the migration process. Unlike adults, juveniles spend more time unburied and foraging, investing energy in growth. Therefore, such environmental conditions favor the establishment of individuals at this stage of a faster growth rate (Dall et al., 1990Dall, W.; Hill, B.J.; Rothlisberg, P.C. and Sharples, D.J. 1990. The biology of the Penaeidae. In: J.H.S. Blaxter and A.J. Southward (eds), Advances in Marine Biology, 27: 1-489. Academic Press, London.).

The present study confirmed that monitoring environmental fluctuations is essential for understanding the distribution patterns of juveniles of F. brasiliensis and F. paulensis. We conclude that variation in rainfall was a key factor in determining the annual presence of juveniles in the marine coastal area. When there is no El Niño, the current shrimp closed season (March to May) is appropriate because it covers the main recruitment of both species of Farfantepenaeus. However, in years when the El Niño phenomenon is more intense, the juveniles become vulnerable because these migrate about two months earlier. Our results also showed that the Ubatuba region is extremely important for conservation, establishment and continuity of the life cycle of these important fishery resources.

Acknowledgements

The authors are grateful to FAPESP for providing financial support (Grant Nos. 94/4878-8, 97/12108-6, 97/12106-3, 97/12107-0, 04/07309-8, 09/54672-4) and to the Brazilian National Council for Scientific and Technological Development (CNPq) (Research Scholarship PQ No. 305919/2014-8 awarded to R.C.C.; PQ No. 308653/2014-9 awarded to A.L.C. and PQ No. 302528/2015-6 awarded to A.F.). We are also thankful to the NEBECC co-workers for their help during fieldwork. All sampling in this study has been conducted in compliance with current applicable state and federal laws in Brazil.

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  • 1
    This article is part of the special series offered by the Brazilian Crustacean Society in honor to Nilton José Hebling in recognition of his dedication and contributions to the development of carcinology in Brazil.
  • 2
    Guest Editors: Maria Lúcia Negreiros-Fransozo and Adilson Fransozo

Publication Dates

  • Publication in this collection
    2016

History

  • Received
    03 Mar 2016
  • Accepted
    17 July 2016
Sociedade Brasileira de Carcinologia Instituto de Biociências, UNESP, Campus Botucatu, Rua Professor Doutor Antônio Celso Wagner Zanin, 250 , Botucatu, SP, 18618-689 - Botucatu - SP - Brazil
E-mail: editor.nauplius@gmail.com