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Juvenile fish use of the shallow zone of beaches of the Cananéia-Iguape coastal system, southeastern Brazil

Abstract

The purpose of the present study is to describe the juvenile fish use of the shallow zone of beaches of the Cananéia-Iguape coastal system, São Paulo, Brazil, analyzing its occurrence period and the patterns of utilization for the most abundant species. Using a beach seine monthly for one year, we sampled 13861 individuals, of 57 species and 24 families. The fish species used the study area for different proposes: Atherinella brasiliensis was sampled in all phases of gonadal development and considered as resident, juveniles of Trachinotus goodei used the beaches for growth and juveniles of Mugil curema and Mugil liza used the beaches as a route from the ocean to the estuary. Our results showed the importance of the sandy beaches for juvenile fish, especially in spring and summer when most juveniles occur and recruit. Unfortunately, this is the period of the most intense tourist activity. As many of the species studied are commercially important, this study highlighted the necessity of coastal habitat preservation for better fishery management.

Descriptors:
Ichthyofauna; Seasonality; Recruitment; Surf zone

Resumo

O objetivo do presente estudo é descrever o uso por peixes juvenis da zona rasa de praias arenosas do sistema costeiro Cananéia-Iguape, São Paulo, Brasil, analisando o período de ocorrência e o padrão de utilização das espécies mais abundantes na área. Utilizando uma rede de arrasto de praia (picaré) mensalmente ao longo de um ano, foram amostrados 13861 indivíduos, pertencentes a 57 espécies e 24 famílias. As espécies analisadas utilizaram a área estudada com diferentes finalidades: Atherinella brasiliensis foi amostrada em todas as fases do desenvolvimento gonadal e, portanto, considerada como residente, juvenis de Trachinotus goodei utilizaram as praias para o crescimento, enquanto os juvenis de Mugil curema e Mugil liza como rota de migração do oceano para o estuário. Nossos resultados mostraram a importância das praias arenosas para peixes juvenis, principalmente na primavera e no verão, quando a maioria dos juvenis recruta na área, e coincide com o período de maior impacto pelos turistas. Como muitas espécies analisadas são comercialmente importantes, ressalta-se ainda a importância de preservação desses habitats costeiros para um melhor manejo pesqueiro.

Descritores:
Ictiofauna; Sazonalidade; Recrutamento; Zona de arrebentação

INTRODUCTION

Environmental conditions have a direct effect on recruitment and, consequently, on population size. Habitats with inadequate physical, chemical or biological environmental conditions for fish can cause a reduction in fecundity, in individual growth rate and an increase in mortality (WENER, 2002WENER, R. G. Habitat Requeriments. In: FUIMAN, L. A.; WENER, R. G. (Eds.). Fishery Science: The unique contributions of early life history. United Kingdom: Blackwell Science, 2002. p. 161-182.). The recognition and preservation of habitats that favor the survival of fish is clearly important to maintain their stocks. However, fish may experience different habitats, from spawning to maturity (Triangle Migration Hypothesis -HARDEN JONES, 1968HARDEN JONES, F. R. Fish migration. London: Edward Arnold, 1968. 325 p.). Nevertheless, it is in the initial phase of the life cycle that environmental conditions may exert a greater influence on fish survival, because, among many other factors, it is at this stage that the organisms are more vulnerable to environmental changes and have limited swimming ability to move, by themselves, to a more suitable habitat (HJORT, 1914HJORT, J. Fluctuations in the great fisheries of northern Europe viewed in the light of biological research. J. Cons-Cons. Perm. Int. Explor. Mer., v. 20, p. 1-228, 1914.).

The process of adding new individuals to a specific stage of the species' life cycle is known as recruitment (JENNINGS et al., 2001JENNINGS, S.; KAISER, M. J.; REYNOLDS, J. D. Marine Fisheries Ecology. USA: Blackwell Science, 2001.). Thus, the survival of juveniles and larvae is related to success in the recruitment of individuals to the adult stock, which in turn is related to the population size. Knowledge of possible environmental factors and human activities that affect fish survival, especially in the initial stages of development, is important for fisheries management, coastal management and species conservation.

The surf zone of sandy beaches is considered an important growth and feeding area for many fish species (MCLACHLAN et al., 1981MCLACHLAN, A., ERASMUS, T., VAN DER HORST, G., ROSSOUW G., LASIAK, T. A.; MCGMYNNE, L. Sand beach energetics: an ecosystem approach towards a high energy interface Estuar. Coast. Shelf Sci., v. 13, n. 1 p. 11-25, 1981.). Juvenile fish recruit in the surf zone because this area provides rich food resources such as components of zooplankton and benthic macrofauna and protection against predators provided by the shallowness, turbidity and turbulence of these areas (e.g. LASIAK, 1981LASIAK, T. A. Nursery grounds of juvenile teleosts: evidence from the surf-zone of King's Beach, Port Elizabeth. S. Afr. J. Mar. Sci., v. 77, p. 388-390, 1981.; CLARK et al., 1996CLARK, B. M.; BENNETT, B. A.; LAMBERT, S. J. Factors affecting spatial variability in seine net catches of fish in the surf zone of False Bay, South Africa. Mar. Ecol. Prog. Ser., v. 131, p. 17-34, 1996b.; PESSANHA; ARAÚJO, 2003PESSANHA, A. L. M.; ARAÚJO, F. G. Spatial, temporal and diel variations of fish assemblages at two sandy beaches in the Sepetiba Bay, RJ. Estuar. Coast. Shelf Sci., v. 57, n. 5-6, p. 817-828, 2003.; VASCONCELLOS et al., 2007VASCONCELLOS, R. M.; SANTOS, J. N. de S.; SILVA, M. A.; ARAÚJO, F. G. Efeito do grau de exposição às ondas sobre a comunidade de peixes juvenis em praias arenosas do Município do Rio de Janeiro, Brasil. Biota Neotrop., v. 7, n. 1, p. 93-100, 2007.). Furthermore, beaches located adjacent to estuaries, as are the beaches that we studied, are considered migration routes of many larvae and juvenile fish, which spend one or more phases of their life cycle within estuaries (COWLEY et al., 2001COWLEY, P. D.; WHITFIELD, A. K.; BELL, K. N. I. The surf zone ichthyoplankton adjacent to an intermittently open estuary, with evidence of recruitment during marine overwash events. Estuar. Coast. Shelf Sci., v. 52, n. 3, p. 339-348, 2001.; WATT- PRINGLE; STRYDOM, 2003WATT- PRINGLE, P.; STRYDOM, N. A. Habitat use by larval fishes in a temperate South African surf zone. Estuar. Coast. Shelf Sci., v. 58, n.4, p. 765-774, 2003.).

Most studies of the ichthyofauna of the shallow zone of beaches analyze the community, with no focus on each population individually. Thus, a lot of information about each species is lost, making it difficult to relate fish spawning and juvenile recruitment. The purpose of the present study is to describe the juvenile fish recruitment in the shallow zone of the beaches of the Cananéia-Iguape Coastal System, analyzing period of occurrence and the patterns of use for the most abundant sampled species.

MATERIAL AND METHODS

Study Site

The Cananéia-Iguape coastal system is located on the southern coast of São Paulo State, between the latitudes of 24º40'S and 25º10'S (Figure 1). It is considered the most protected coastal zone in São Paulo State. The average an nual temperature is 23.8 ºC, and the average annual precipitation is 2300 mm (SILVA, 1989SILVA, I. F. Dados climatológicos de Cananéia e Ubatuba (Estado de São Paulo). Série de 1956-1985. Bol. Climatol., v.6, p.1-21, 1989.). There is a mixed tide with an amplitude of 0.81 m (MESQUITA; HARARI, 1983MESQUITA, A. R.; HARARI, J. Tides and tide gauges of Cananéia and Ubatuba - Brazil (Lat 24º). Relat. Int. Inst. Oceanogr., São Paulo, v. 11, p. 1-14, 1983.).

Figure 1.
Location of the sampled beaches at Comprida Island and at Cardoso Island State Park, southeast Brazil.

A recent data compilation indicated that this region contains at least 246 fish species (CONTENTE, 2013CONTENTE, R. F. Padrões ecológicos locais e multidecadais da ictiofauna do estuário Cananéia-Iguape. 185 f. Tese (Doutorado em Oceanografia Biológica)- Instituto Oceanográfico, Universidade de São Paulo, São Paulo, 2013.). At Cardoso Island State Park (Figure 1), the spatio-temporal variation in the surf-zone fish community was studied by FAVERO and DIAS (2013)FAVERO, J. M.; DIAS. J. F. Spatio-temporal variation in surf zone fish communities at Ilha do Cardoso State Park, São Paulo, Brazil. Lat. Am. J. Aquat. Res., v. 41, n. 2, p. 239-253, 2013..

Coastal and estuarine fisheries are an important socioeconomic activity for the inhabitants of towns bordering the Cananéia-Iguape coastal system (MENDONÇA; KATSURAGAWA, 1997MENDONÇA, J. T.; KATSURAGAWA, M. Desembarque da pesca costeira em Cananéia (São Paulo), Brasil, durante 1995 e 1996. Nerítica, v. 11, p.1965-190, 1997.; 2001MENDONÇA, J. T.; KATSURAGAWA, M. Caracterização da pesca artesanal no complexo estuarino-lagunar de Cananéia-Iguape, Estado de São Paulo, Brasil (1995-1996). Acta Sci., v.23, n.2, p. 535-547, 2001.). The main fish resources of the region are: Anchoviella lepidentostole, Macrodon ancylodon, Mugil liza, Mugil curema, Micropogonias furnieri and Genidens barbus (MENDONÇA; MIRANDA, 2008MENDONÇA, J. T.; MIRANDA, L. V. Estatística pesqueira do litoral sul do estado de São Paulo: subsídios para a gestão compartilhada. Pan-Am. J. Aquat. Sci., v.3, n.3, p.152-173, 2008.).

Sampling methods

The beaches studied were located in the Cardoso Island State Park and on Comprida Island (Figure 1). Although no studies were found that characterize the morphology of the beaches studied, during the surveys it was observed that the further into the channel, the smaller the wave heights and more silty the sediment.

Fish were sampled monthly over one year, from February 2009 to January 2010. On each beach four consecutive hauls of approximately 30 m each were made using a beach seine net, 9 m long, 1.5 m high with a stretched mesh size of 5 mm when pulled by hand. All samples were collected at low and high spring tide. Low tide was sampled at its morning peak while the high tide was usually sampled during the afternoon, at a time close to its peak. At the start of the first haul and at the end of the last one, on each beach, the water temperature was measured with a mercury thermometer and the water salinity with a refractometer.

All fish collected were identified following FIGUEIREDO and MENEZES (1978FIGUEIREDO, J. L.; MENEZES, N. A. Manual de peixes marinhos do sudeste do Brasil. II. Teleostei (1). São Paulo: Museu de Zoologia da Universidade de São Paulo, 1978. 110 p., 1980FIGUEIREDO, J. L.; MENEZES, N. A. Manual de peixes marinhos do sudeste do Brasil. III. Teleostei (2). São Paulo: Museu de Zoologia da Universidade de São Paulo, 1980. 90 p., 2000FIGUEIREDO, J. L.; MENEZES, N. A. Manual de peixes marinhos do sudeste do Brasil. VI. Teleostei (5). São Paulo: Museu de Zoologia da Universidade de São Paulo, 2000. 116 p.), MENEZES and FIGUEIREDO (1980MENEZES, N. A.; FIGUEIREDO, J. L. Manual de peixes marinhos do sudeste do Brasil. IV. Teleostei (3). São Paulo: Museu de Zoologia da Universidade de São Paulo, 1980. 96 p., 1985MENEZES, N. A.; FIGUEIREDO, J. L. Manual de peixes marinhos do sudeste do Brasil. V. Teleostei (4). São Paulo: Museu de Zoologia da Universidade de São Paulo, 1985. 105 p.) and RICHARDS (2006)RICHARDS, W. J. Early stages of Atlantic Fishes: an identification guide for the Western Central North Atlantic. Boca Raton: CRC Press, 2006. 2640p.. Due to the difficulty in identifying juvenile Mugilidae and the lack of taxonomic literature for the specific distinction within this family on the Brazilian southeastern coast, all mugilids collected were separated based on VIEIRA (1991)VIEIRA, J. P. Juvenile Mullets (Pisces: Mugilidae) in the Estuary of Lagoa dos Patos, RS, Brazil. Copeia, v. 2, p. 409-418, 1991.. The following nomenclature was used: Mugil hospes (previously Mugil gaimardianus), and Mugil liza (previously Mugil platanus) according to MENEZES et al. (2010)MENEZES, N. A.; OLIVEIRA, C.; NIRCHIO, N. An old taxonomic dilemma: the identity of the western south Atlantic lebranche mullet (Teleostei: Perciformes: Mugilidae). Zootaxa, v. 2519, p. 59-68, 2010..

Fish were measured to the nearest 1 mm (standard length), except when samples were very large. On these occasions, measurements were restricted to a subsample of 50 individuals per species. The excess was counted and incorporated as number counts. In addition, sex (male, female or not identified) and maturity stages were documented for the subsample through macroscopic observation, according to VAZZOLER (1996)VAZZOLER, A. E. A. M. Biologia da reprodução de peixes teleósteos: Teoria e prática. Maringá: Eduem. 1996. 169p. and DIAS et al. (1998)DIAS, J. F.; PERES-RIOS, E.; CHAVES, P. T. C.; ROSSI-WONGTSCHOWSKI, C. L. D. B. Análise macroscópica dos ovários de teleósteos: problemas de classificação e recomendações de procedimentos. Rev. Bras. Biol., v. 58, n. 1, p. 55-69, 1998..

Data analysis

Analysis of variance (one way ANOVA) was used to test the significance of differences between the monthly abiotic data of water temperature and water salinity. Tukey post-hoc tests were conducted to evaluate which means differed from each other.

All the biological analyses were made using only the eight most-abundant fish species (occurrence greater than 3%), excluding the species sampled only in the larval phase. As there were not enough individuals per species to perform a monthly analysis, the data were grouped per season as: spring = September, October and November; summer = December, January and February, autumn = March, April and May, winter = June, July and August.

To assess whether fish were using the beaches as growth areas, an empirical cumulative distribution function (ECDF) of standard length was performed for each species in each season. Differences in the standard length distribution per season were tested by a permutation test with a confidence level of 99% (p < 0.01).

The analyses were made using the R program (R CORE TEAM, 2012R CORE TEAM. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available from: <http://www.R-project.org/>. Acessed in: 2012.
http://www.R-project.org/...
).

RESULTS

Water temperature varied significantly over the year sampled, especially comparing the warmer months (November-April) with the coldest ones (May-October) (Figure 2). The maximum water temperature was 30.5 ºC in March and the minimum was 18.0 ºC in June and August.

Figure 2.
Monthly variation of water temperature (ºC) recorded in beaches of the Cananéia-Iguape coastal system from February 2009 to January 2010.

Despite the significant difference in water salinity in the months sampled, there was no clear variation pattern in salinity as was observed for water temperature (Figure 3). The salinity variation was probably due to beach localization, tide and rainfall. The maximum water salinity was 36 in June and the minimum was 12 in January.

Figure 3.
Monthly variation of water salinity recorded in beaches of the Cananéia-Iguape coastal system from February 2009 to January 2010.

A total of 13,861 individuals, belonging to 57 species and 24 families, were collected. Of the total, 34 were sampled at both islands, 10 were sampled only at Comprida Island, and 13 only at Cardoso Island. The fish species that were collected only at one island were rare, up to 20 individuals per species. The exception was Choloroscombrus chrysurus, which was sampled only at Cardoso Island and was abundant (N = 145) (Table 1).

Table 1
Monthly number of the fish species sampled in the surf zone of sandy beaches located in the Cananeia-Iguape Coastal System from February 2009 to January 2010

The most-abundant species were: Mugil curema (23.01%), Trachinotus carolinus (21.40%), Mugil hospes (16.12%), Gerreidae larvae (9.46%), Trachinotus goodei (5.18%), Atherinella brasiliensis (4.88%), Harengula clupeola (3.68%) and Mugil liza (3.05%). Atherinella brasiliensis was the only species sampled as adults (N = 170), juveniles (N = 493) and larvae (N = 1), and all the other fish species were sampled only as juveniles.

Carangids were abundant during all seasons. Recruitment of T. goodei juveniles started in spring, when approximately 70 % of fish sampled were of small length (11.5 to 25 mm). An increase in fish size was observed in each season from spring to winter. During the winter no fish smaller than 30 mm were sampled, and a high per centage of individuals larger than 50 mm was recorded (Figure 4). The minimum and the maximum standard length for T. goodei was 11.50 mm and 152 mm, both observed in spring. Trachinotus goodei was more abundant in summer (N = 245), then in autumn (N = 238), followed by spring (N = 164) and winter (N = 71).

Figure 4.
Empirical cumulative distribution function (ECDF) of standard length (SL) of Thachinotus goodei sampled in beaches of the Cananéia-Iguape coastal system from February 2009 to January 2010.

Although the permutation test showed significant differences between the standard lengths in different seasons, no clear pattern of individuals' growth was observed for T. carolinus, as small-sized individuals were abundant during all seasons (Figure 5). The minimum standard length observed was 1.5 mm during winter and the maximum was 70 mm in spring. As observed for T. goodei, T. carolinus was more abundant in summer (N = 1,213), than in autumn (N = 458), followed by spring (N = 359) and winter (N = 128).

Figure 5.
Empirical cumulative distribution function (ECDF) of standard length (SL) of Thachinotus carolinus sampled in beaches of the Cananéia-Iguape coastal system from February 2009 to January 2010.

A small range of standard length was observed for mugilids. Most of them measured from 20 mm to 30 mm. No pattern of individual growth through the seasons was observed due to the small size range. This fact combined with the presence of the individuals in all seasons, suggests a constant input of juveniles during the year, but with greater abundance at different times: M. curema and M. hospes during summer and M. liza during winter (Table 2).

Table 2
Total number of mugilids sampled in the surf zone of the Costal System Cananeia-Iguape from February 2009 to January 2010

Atherinella brasiliensis was the only species with representatives in all phases of gonadal development in the study area (Figure 6). Small-size individuals were abundant in summer, with dominance of the 40 - 60 mm size class. In subsequent seasons, it was possible to observe a significant increase in the size of the individuals (Figure 7). The high abundance of maturing individuals from September to November was related to the high abundance of individuals in the largest size class in spring. Furthermore, 97% of the fish sampled in January were immature, being related to the smallest size class observed in summer (Figure 6 and Figure 7).

Figure 6.
Monthly frequency of occurrence of the gonadal stages of Atherinella brasiliensis sampled in the surf zone of sandy beaches located in the Cananéia-Iguape coastal system from February 2009 to January 2010.
Figure 7.
Empirical cumulative distribution function (ECDF) of standard length (SL) of Atherinella brasiliensis sampled in beaches of the Cananéia-Iguape coastal system from February 2009 to January 2010.

Small-size individuals of H. clupeola were collected only in summer. The greatest abundance of this species occurred in winter, when most of the fish measured from 55 mm to 65 mm. Even though the permutation test showed significant results between the different standard lengths in the different seasons, there was no clear pattern of individuals' growth (Figure 8).

Figure 8.
Empirical cumulative distribution function (ECDF) of standard length (SL) of Harengula clupeola sampled in beaches of the Cananéia-Iguape coastal system from February 2009 to January 2010.

DISCUSSION

Closed areas where juveniles aggregate have often been assumed to benefit recruitment by reducing the mortality of undersized individuals (WRIGHT et al., 2010WRIGHT, P. J.; TOBIN, D.; GIBB, F. M.; GIBB, I. M. Assessing nursery contribution to recruitment: relevance of closed areas to haddock Melanogrammus aeglefinus. Mar. Ecol. Prog. Ser., v. 400, p. 221-232, 2010.). Surf zones of sandy beaches have this function, as resident fish are a minority and most species present are represented by young seasonal or sporadic migrants (MCLACHLAN, 1983MCLACHLAN A. Sandy beach ecology- a review. In: MACLACHLAN A.; ERASMUS, T. (Eds). Sandy beaches as ecosystems. Junk: The Hague, 1983. p.321-380.).

Considering that resident species are only those that spend their entire life cycle and the whole year in the same area, only A. brasiliensis can be considered as resident at the beaches sampled, even though they undergo some little migration from the beach to the river (FERNANDEZ, 2007FERNANDEZ, W. S. Dinâmica populacional de Atherinella brasiliensis (Quoy & Gaimard, 1824) da Praia de Itamambuca, Ubatuba. 144 f. Dissertation (Master in Biological Oceanography)- Instituto Oceanográfico, Universidade de São Paulo, São Paulo, 2007.). No resident species were observed by FÉLIX et al. (2007a)FÉLIX, F. C.; SPACH, H. L.; Moro, P. S.; HACKRADT, C. W.; QUEIROZ, G. M. L. N.; HOSTIM-SILVA, M. Icthyofauna composition across a wave-energy gradient on southern Brazil beaches. Braz. J. Oceanogr., v. 55, n. 4, p. 281-292, 2007a. on the beaches of Pontal do Sul, in Paraná State. MODDE (1980)MODDE, T. Growth and residency of juvenile fishes within a surf zone habitat in the Gulf of México. Gulf Res. Rep., v. 6, n. 4, p. 377-385, 1980. classified six fish species as resident in the surf zone of beaches of the Gulf of Mexico, but there were no analyses of the maturity stage, and the classification was based only on the individuals' size classes and the monthly frequency of occurrence. MODDE (1980)MODDE, T. Growth and residency of juvenile fishes within a surf zone habitat in the Gulf of México. Gulf Res. Rep., v. 6, n. 4, p. 377-385, 1980. points out that more than half of the fish caught were juvenile migrants which may have been using the area as a refuge or as migratory route. According to LAYMAN (2000)LAYMAN, C. A. Fish Assemblage Structure of the Shallow Ocean Surf-Zone on the Eastern Shore of Virginia Barrier Islands. Estuar. Coast. Shelf Sci., v.51, n. 2, p. 201-213, 2000., most of the fish species collected were classified as seasonal juveniles using the shallow water as nurseries, or transient adults, which were more abundant in other marine habitats.

No matter the fishing gear used, all the species analyzed in this study were also sampled inside the Cananéia-Iguape coastal system or close to its mouth (ZANI-TEIXEIRA, 1983ZANI-TEIXEIRA, M. L. Contribuição ao conhecimento da ictiofauna da Baía do Trapandé, Complexo Estuarino Lagunar de Cananéia, São Paulo. 254 f. Dissertation (Master in Biological Oceanography)- Instituto Oceanográfico, Universidade de São Paulo, São Paulo, 1983.; MACIEL, 2001MACIEL, N. A. L. Composição, Abundância e distribuição espaço-temporal da ictiofauna do Complexo Estuarino Lagunar de Iguape-Cananéia- São Paulo, Brasil. 252 f. Thesys (Doctor in Biological Oceanography)- Instituto Oceanográfico, Universidade de São Paulo, São Paulo, 2001.). Harengula clupeola, M. curema, T. carolinus and T goodei were also sampled at Bom Abrigo Island, an island located just outside the coastal system studied (SAUL; CUNNINGHAM, 1995SAUL, A. C.; CUNNINGHAM, P. T. M. Comunidade ictiofaunística da ilha do Bom Abrigo, Cananéia.Brasil. 2-Lanço. Arq. Biol. Tecnol., v. 38, n. 4, p. 1053-1069, 1995.). In addition, Cananéia fisheries' landing data reported the occurrence of T. carolinus and T. goodei outside the estuary (MENDONÇA; KATSURAGAWA, 1997MENDONÇA, J. T.; KATSURAGAWA, M. Desembarque da pesca costeira em Cananéia (São Paulo), Brasil, durante 1995 e 1996. Nerítica, v. 11, p.1965-190, 1997.), while mugilids were an important estuarine fishery resource in the Cananéia-Iguape coastal system (MENDONÇA; KATSURAGAWA, 2001MENDONÇA, J. T.; KATSURAGAWA, M. Caracterização da pesca artesanal no complexo estuarino-lagunar de Cananéia-Iguape, Estado de São Paulo, Brasil (1995-1996). Acta Sci., v.23, n.2, p. 535-547, 2001.). These facts reinforce the idea that the fish species studied are recruited as young-of-the-year on these beaches, and use the beaches only during a short time. In general, the main inter-season changes in abundance and community structure were due to the variation of the key species and reflected the different times of their recruitment (SELLESLAGH; AMARA, 2008SELLESLAGH, J.; AMARA, R. Inter-season and interannual variations in fish and macrocrustacean community structure on an eastern English Channel sandy beach: influence of environmental factors. Estuar. Coast. Shelf Sci., v. 77, n.4, p.721-730, 2008.).

The genus Trachinotus inhabits coastal areas, frequently in the surf zone of beaches (MENEZES; FIGUEIREDO, 1980MENEZES, N. A.; FIGUEIREDO, J. L. Manual de peixes marinhos do sudeste do Brasil. IV. Teleostei (3). São Paulo: Museu de Zoologia da Universidade de São Paulo, 1980. 96 p.). Several studies of Brazilian beaches (GIANNINI; PAIVA FILHO, 1995GIANNINI, R.; PAIVA FILHO, A. M. Análise comparativa da ictiofauna da zona de arrebentação de praias arenosas do Estado de São Paulo, Brasil. Bol. Inst. Oceanogr., v. 43, n. 2, p. 141-152, 1995.; GODEFROID et al., 2003GODEFROID, R. S.; SPACH, H. L.; SANTOS, C.; MACLAREN, G.; SCHWARZ JR, R.; A fauna de peixes da praia do Balneário Atami, Paraná, Brasil. Atlântica., v. 25, n. 2, p. 147-161, 2003.; VASCONCELLOS et al., 2007VASCONCELLOS, R. M.; SANTOS, J. N. de S.; SILVA, M. A.; ARAÚJO, F. G. Efeito do grau de exposição às ondas sobre a comunidade de peixes juvenis em praias arenosas do Município do Rio de Janeiro, Brasil. Biota Neotrop., v. 7, n. 1, p. 93-100, 2007.; GAELZER; ZALMON, 2008GAELZER, L. R.; ZALMON, I. R. Diel variation of fish community in sandy beaches of southeastern Brazil. Braz. J. Oceanogr., v. 56, n. 1, p. 23-39, 2008.; FAVERO; DIAS, 2013FAVERO, J. M.; DIAS. J. F. Spatio-temporal variation in surf zone fish communities at Ilha do Cardoso State Park, São Paulo, Brazil. Lat. Am. J. Aquat. Res., v. 41, n. 2, p. 239-253, 2013.) and beaches elsewhere (MODDE, 1980MODDE, T. Growth and residency of juvenile fishes within a surf zone habitat in the Gulf of México. Gulf Res. Rep., v. 6, n. 4, p. 377-385, 1980.; SANTOS; NASH, 1995SANTOS, R. S.; NASH, R. D. M. Seasonal changes in a sandy beach fish assemblage at Porto Pim, Faial, Azores. Estuar. Coast. Shelf Sci., v. 41, n. 6, p. 579-591, 1995.; LAYMAN, 2000LAYMAN, C. A. Fish Assemblage Structure of the Shallow Ocean Surf-Zone on the Eastern Shore of Virginia Barrier Islands. Estuar. Coast. Shelf Sci., v.51, n. 2, p. 201-213, 2000.) indicate high abundance of juveniles of this genus in such habitats. However, information on the spawning sites and seasons remains sparse, which makes it difficult to interpret the Trachinotus recruitment pattern in the study area.

Trachinotus goodei usually occurs in the surf zone of sandy beaches forming large shoals associated with saline waters, while T. carolinus occurs in small or large shoals along sandy beaches, inlets and bays with brackish water (CARPENTER, 2002CARPENTER, K. E. (Ed.) The living marine resource of the western central Atlantic. Volume 3: Bony fishes part 2 (Opistognathidae to Molidae), sea turtles and marine mammals. Food Agriculture Organization of the United Nations. Rome, 2002.). Apparently, juvenile T. goodei recruit in the study area mainly in spring, showing a clear pattern of seasonal growth during the year, while T. carolinus recruits throughout the year, as previously described by FÉLIX et al. (2007b)FÉLIX, F. C.; SPACH, H. L.; MORO, P. S.; SCHWARZ JR. R.; SANTOS, C.; HACKRADT, C. W.; HOSTIM-SILVA, M. Utilization pattern of surf zone inhabiting fish from beaches in Southern Brazil. Pan-Am. J. Aquat. Sci., v. 2, n. 1, p. 27-39, 2007b..

As T. goodei were sampled in length classes larger than those of T. carolinus, it is possible to conclude that the beach seine selectivity did not influence the capture of T. carolinus. This confirms that T. carolinus larger than 60 mm migrate to deeper water (FIELDS, 1962FIELDS, H. M. Pompanos (Trachinotus spp.) of South Atlantic coast of United States. Fish. Bull., v. 207, n. 62, p. 189-222, 1962.; MODDE, 1980MODDE, T. Growth and residency of juvenile fishes within a surf zone habitat in the Gulf of México. Gulf Res. Rep., v. 6, n. 4, p. 377-385, 1980.; FÉLIX et al., 2007aFÉLIX, F. C.; SPACH, H. L.; Moro, P. S.; HACKRADT, C. W.; QUEIROZ, G. M. L. N.; HOSTIM-SILVA, M. Icthyofauna composition across a wave-energy gradient on southern Brazil beaches. Braz. J. Oceanogr., v. 55, n. 4, p. 281-292, 2007a.). Probably the spawning o T. carolinus occurs in oceanic waters (CARPENTER, 2002CARPENTER, K. E. (Ed.) The living marine resource of the western central Atlantic. Volume 3: Bony fishes part 2 (Opistognathidae to Molidae), sea turtles and marine mammals. Food Agriculture Organization of the United Nations. Rome, 2002.). The fishing method probably was size selective for T. goodei, because mature individuals of this species had previously been sampled at Atami Beach, in southern Brazil (GODEFROID et al., 2003GODEFROID, R. S.; SPACH, H. L.; SANTOS, C.; MACLAREN, G.; SCHWARZ JR, R.; A fauna de peixes da praia do Balneário Atami, Paraná, Brasil. Atlântica., v. 25, n. 2, p. 147-161, 2003.) and, during our sampling days, several people fishing with hook and line were observed catching T. goodei larger than those captured with the beach seine.

Mugilids are coastal fishes that are found abundantly in estuaries. Small-size individuals are very abundant in the shallow zone of sandy beaches, mainly near river mouths (MENEZES; FIGUEIREDO, 1985MENEZES, N. A.; FIGUEIREDO, J. L. Manual de peixes marinhos do sudeste do Brasil. V. Teleostei (4). São Paulo: Museu de Zoologia da Universidade de São Paulo, 1985. 105 p.). Usually, they spawn in oceanic waters, but afterwards move into coastal areas, entering estuaries and rivers, where they settle (MENEZES; FIGUEIREDO, 1985MENEZES, N. A.; FIGUEIREDO, J. L. Manual de peixes marinhos do sudeste do Brasil. V. Teleostei (4). São Paulo: Museu de Zoologia da Universidade de São Paulo, 1985. 105 p.; VIEIRA; SCALABRIN, 1991VIEIRA, J. P.; SCALABRIN, C. Migração reprodutiva da "Tainha" (Mugil platanus GUNTHER, 1980) no sul do Brasil. Atlântica, v. 13, n. 1, p. 131-141, 1991.; CHANG, 2000CHANG, C. W.; TZENG, W. N.; LEE, Y. C. Recruitment and Hatching Dates of Grey Mullet (Mugil cephalus L.) Juveniles in the Tanshui Estuary of Northwest Taiwan. Zool. Stud., v. 39, n. 2, p. 99-106, 2000.; SILVA, 2007SILVA, F. M. S. Biologie, Pêche et Dynamique de la Population de Mulet Blanc (Mugil curema, Valenciennes, 1836) de Pernambuco, Brasil. 260 f. Thesis (Doctoral in Biological Oceanography)- Université de Bretagne Occidentale, França, 2007.).

In the present study, a small variation was noticed in the individuals' lengths throughout the year, but there was no clear pattern of seasonal growth for the mugilid species. The higher abundance of M. curema and M. hospes during summer, and of M. liza during winter was also observed in a Brazilian coastal lagoon (VIEIRA, 1991VIEIRA, J. P. Juvenile Mullets (Pisces: Mugilidae) in the Estuary of Lagoa dos Patos, RS, Brazil. Copeia, v. 2, p. 409-418, 1991.). There was also a greater abundance of M. liza juveniles during July and September in the surf zone of a beach located in southern Brazil (VIEIRA; SCALABRIN, 1991VIEIRA, J. P.; SCALABRIN, C. Migração reprodutiva da "Tainha" (Mugil platanus GUNTHER, 1980) no sul do Brasil. Atlântica, v. 13, n. 1, p. 131-141, 1991.).

As we obtained specimens of other species larger than 100 mm standard length, it is believed that the small size range in which most mugilids were collected is not caused by the beach seine selectivity. Two hypotheses have been suggested to explain this small size range: 1) Mugilids are fast swimmers (RULIFSON, 1977RULIFSON, R. A. Temperature and water velocity effects on the swimming performances of young-of-the-year striped mullet (Mugil cephalus), spot (Leiostomus xanthurus), and pinfish (Lagodon rhomboides). J. Fish. Res. Board Can., v. 34, p. 2316-2322, 1977.), so bigger individuals can avoid the beach seine net, which is pulled by hand, at low speed. 2) Small-size mugilids use the beaches sampled as a route from the ocean to the estuary.

The reproductive period varies according to species and area studied. The spawning period of M. liza is from September to November in Paranaguá Bay (ESPER et al., 2001ESPER, M. L. P.; MENEZES, M. S.; ESPER, W. Época reprodutiva de Mugil platanus (Günther, 1880), Pisces Mugilidae da Baia de Paranaguá (Paraná, Brasil). Acta Biol. Par., v. 30, n. 1, 2, 3, 4, p. 5-17, 2001.) and from June to October in Cananéia (ANDRADE-TALMELLI et al., 1996ANDRADE-TALMELLI, E. F. A.; ROMAGOSA, E.; NARAHARA, M. Y.; GODINHO, H. M. Características reprodutivas de Tainha Mugil platanus (Teleostei, Perciformes, Mugilidae) da região Estuarino-Lagunar de Cananéia, São Paulo. Rev. Ceres, v. 43, n. 246, p. 165-185, 1996.). VIEIRA and SCALABRIN (1991)VIEIRA, J. P.; SCALABRIN, C. Migração reprodutiva da "Tainha" (Mugil platanus GUNTHER, 1980) no sul do Brasil. Atlântica, v. 13, n. 1, p. 131-141, 1991. reported that M. liza migration from the Patos Lagoon (south Brazil) to oceanic waters starts in April and May (autumn), with the spawning peak in May and June. Those authors also indicated that the juvenile recruitment occurs throughout the year, especially during the winter and spring.

The Mugil curema spawning period is from February to May in the Gulf of Mexico (AGUIRRE; GALLARDO-CABELLO, 2004AGUIRRE, A. L. I.; GALLARDO-CABELLO, M. Reproduction of Mugil cephalus and M. curema (Pisces: Mugilidae) from a coastal lagoon in the Gulf of México. Bull. Mar. Sci., v. 75, n. 1, p. 37-49, 2004.), while along the coast of São Paulo State, M. curema from the Cananéia-Iguape coastal system and from the Santos estuary showed the beginning of gonadal maturation in October, which extended to April, with two annual spawning events, one in April and another in November (FERNANDEZ; DIAS, 2013FERNANDEZ, W. S.; DIAS, J. F. Aspects of the reproduction of Mugil curema Valenciennes, 1836 in two coastal systems in southeastern Brazil. Trop. Zool., v. 26, n. 1, p. 15-32, 2013.), whereas around Santos it occurred in late spring and early summer (CERGOLE, 1986CERGOLE, M. C. Aspectos sobre a biologia de M. curema VALLENCINES, 1836 (Pisces, Mugilidae) no estuário de São Vicente, SP. 272 f. Dissertation (Master in Biological Oceanography)- Instituto Oceanográfico, Universidade de São Paulo, São Paulo, 1986.; FERREIRA, 1989FERREIRA, L. I. Estudos de aspectos da reprodução de Mugil curema Vallenciennes, 1836 (Pisces, Mugilidae) no estuário de São Vicente. 90 f. Dissertation (Master in Biological Oceanography)- Instituto Oceanográfico, Universidade de São Paulo, São Paulo, 1989.). Spawning individuals migrated offshore from a coastal lagoon in Venezuela from September until January, and the juvenile fish recruited to the lagoon mainly between March and June (MARÍN et al., 2003MARÍN, B. J.; QUINTERO A.; BUSSIÈRE, D.; DODSON, J.J. Reproduction and recruitment of White Mullet (Mugil curema) to a tropical lagoon (Margarita Island, Venezuela) as revealed by otolith microstructure. Fish. Bull., v. 101, n. 4, p. 809-821, 2003.). Thus, the gap between the spawning period described for M. liza and M. curema and the juvenile recruitment period at the beaches sampled, corroborates the second hypothesis presented above.

Atherinella brasiliensis was the only species represented by mature and spent females. However, no hydrated oocytes were observed. As oocyte hydration is a short term process (less than 8 hours) and indicates imminent spawning (HUNTER; GOLDBERG, 1980HUNTER, J. R.; GOLDBERG, S. R. Spawning incidence and batch fecundity in Northern Anchovy Engraulis mordax. Fish. Bull., v. 77, n. 3, p.641-652, 1980.; DIAS et al., 1998DIAS, J. F.; PERES-RIOS, E.; CHAVES, P. T. C.; ROSSI-WONGTSCHOWSKI, C. L. D. B. Análise macroscópica dos ovários de teleósteos: problemas de classificação e recomendações de procedimentos. Rev. Bras. Biol., v. 58, n. 1, p. 55-69, 1998.), it is possible to conclude that A. brasiliensis does not use the surf zone to spawn during the daytime or leaves the surf zone for final maturation. As this species migrates daily, leaving the Itamambuca beach surf zone and going to the Itamambuca River to spawn (FERNANDEZ, 2007FERNANDEZ, W. S. Dinâmica populacional de Atherinella brasiliensis (Quoy & Gaimard, 1824) da Praia de Itamambuca, Ubatuba. 144 f. Dissertation (Master in Biological Oceanography)- Instituto Oceanográfico, Universidade de São Paulo, São Paulo, 2007.), in the study area the spawning probably occurs inside the estuary or in a small river close to the most internal beach at Cardoso Island (beach number 4 in Figure 1). Additionally, Atherinopsidae eggs have filaments that are used to stick in the aquatic vegetation (HUAQUÍN, 1980; MARÍN et al., 1995MARÍN, B. M.; DIAZ, O.; BRICEÑO, R. Aspectos descriptivos de los ovócitos y postlarva de tinicalo Xenomelaniris brasiliensis (Quoy & Gaimard) (Pisces: Atherinidae). Bol. Inst. Oceanogr., v. 34, n. 1/2, p. 59-68, 1995.). This helps to understand why the females do not spawn at the beaches sampled, as there is no vegetation to serve as substrate for eggs.

Atherinella brasiliensis spawns throughout the year in the Cananéia-Iguape coastal system, more intensely during winter and spring (PERES-RIOS, 2001PERES-RIOS, E. Papel do estuário no ciclo de vida das espécies dominantes da ictiofauna do Complexo Estuarino. Lagunar de Cananéia, Iguape. 128 f. Thesis (Doctoral in Biological Oceanography)- Instituto Oceanográfico, Universidade de São Paulo, São Paulo, 2001.). This may be related to the juveniles' recruitment at the beaches sampled, during summer. PESSANHA and ARAÚJO (2001)PESSANHA, A. L. M.; ARAÚJO F. G. Recrutamento do peixe-rei Xenomelaniris brasiliensis (Atheriniformes, Atherinopsidae), na margem continental da Baía de Sepetiba, Rio de Janeiro, Brasil. Rev. Bras. Zool., v. 18, n. 4, p. 1265-1274, 2001. and FERNANDEZ (2007)FERNANDEZ, W. S. Dinâmica populacional de Atherinella brasiliensis (Quoy & Gaimard, 1824) da Praia de Itamambuca, Ubatuba. 144 f. Dissertation (Master in Biological Oceanography)- Instituto Oceanográfico, Universidade de São Paulo, São Paulo, 2007. also indicated that summer was the recruitment season of A. brasiliensis on beaches. In the Paranaguá Bay estuarine complex, A. brasiliensis distribution among size classes varied significantly across seasons, with larger fish prevailing during winter and spring (reproductive period), resulting in the high abundance of recruits of the year during the summer (FÁVARO et al., 2003FÁVARO, L. F.; LOPES, S. C. G.; SPACH, H. L. Reprodução do peixe, Atherinella brasiliensis (Quoy & Gaimard) (Atheriniformes, Atherinidae), em uma planície de maré adjacente à gamboa do Baguaçu, Baía de Paranaguá, Paraná, Brasil. Rev. Bras. Zool., v. 20, n. 3, p. 501-506, 2003.; CONTENTE et al., 2011CONTENTE, R. F.; STEFANONI, M. F.; SPACH, H. L. Feeding ecology of the Brazilian silverside Atherinella brasiliensis (Atherinopsidae) in a sub-tropical estuarine ecosystem. J. Mar. Biol. Assoc. U.K., v. 91, n. 6, p. 1197-1205, 2011.). The same patterns of annual growth and recruitment were observed in the area here studied.

Even with the occurrence of Sardinella brasiliensis and Opisthonema oglinum, H. clupeola was the only abundant clupeid species. The high abundance of H. clupeola in the surf zone of Brazilian sandy beaches has previously been reported by several authors (GIANNINI; PAIVA FILHO, 1995GIANNINI, R.; PAIVA FILHO, A. M. Análise comparativa da ictiofauna da zona de arrebentação de praias arenosas do Estado de São Paulo, Brasil. Bol. Inst. Oceanogr., v. 43, n. 2, p. 141-152, 1995.; PESSANHA; ARAÚJO, 2003PESSANHA, A. L. M.; ARAÚJO, F. G. Spatial, temporal and diel variations of fish assemblages at two sandy beaches in the Sepetiba Bay, RJ. Estuar. Coast. Shelf Sci., v. 57, n. 5-6, p. 817-828, 2003.; VASCONCELLOS et al., 2007VASCONCELLOS, R. M.; SANTOS, J. N. de S.; SILVA, M. A.; ARAÚJO, F. G. Efeito do grau de exposição às ondas sobre a comunidade de peixes juvenis em praias arenosas do Município do Rio de Janeiro, Brasil. Biota Neotrop., v. 7, n. 1, p. 93-100, 2007.; GAELZER; ZALMON, 2008GAELZER, L. R.; ZALMON, I. R. Diel variation of fish community in sandy beaches of southeastern Brazil. Braz. J. Oceanogr., v. 56, n. 1, p. 23-39, 2008.), especially during the winter, as in the present study (SAUL; CUNNINGHAM, 1995SAUL, A. C.; CUNNINGHAM, P. T. M. Comunidade ictiofaunística da ilha do Bom Abrigo, Cananéia.Brasil. 2-Lanço. Arq. Biol. Tecnol., v. 38, n. 4, p. 1053-1069, 1995.; FÉLIX et al., 2007aFÉLIX, F. C.; SPACH, H. L.; Moro, P. S.; HACKRADT, C. W.; QUEIROZ, G. M. L. N.; HOSTIM-SILVA, M. Icthyofauna composition across a wave-energy gradient on southern Brazil beaches. Braz. J. Oceanogr., v. 55, n. 4, p. 281-292, 2007a.). This species has its juvenile phase in the Cananéia-Iguape coastal system, mainly at the beaches (PERES-RIOS, 2001PERES-RIOS, E. Papel do estuário no ciclo de vida das espécies dominantes da ictiofauna do Complexo Estuarino. Lagunar de Cananéia, Iguape. 128 f. Thesis (Doctoral in Biological Oceanography)- Instituto Oceanográfico, Universidade de São Paulo, São Paulo, 2001.).

Although juveniles of Gerreidae are among the most abundant groups in the coastal ecosystems, including those caught in beach seine samples (ARAÚJO; SANTOS, 1999ARAÚJO, F. G.; SANTOS, A. C. A. Distribution and recruitment of Mojarras (Perciformes, Gerreidae) in the continental margin of Sepetiba Bay, Brazil. Bull. Mar. Sci., v. 65, n. 2, p. 431-439, 1999.; FÉLIX et al., 2007aFÉLIX, F. C.; SPACH, H. L.; Moro, P. S.; HACKRADT, C. W.; QUEIROZ, G. M. L. N.; HOSTIM-SILVA, M. Icthyofauna composition across a wave-energy gradient on southern Brazil beaches. Braz. J. Oceanogr., v. 55, n. 4, p. 281-292, 2007a.; 2007bFÉLIX, F. C.; SPACH, H. L.; MORO, P. S.; SCHWARZ JR. R.; SANTOS, C.; HACKRADT, C. W.; HOSTIM-SILVA, M. Utilization pattern of surf zone inhabiting fish from beaches in Southern Brazil. Pan-Am. J. Aquat. Sci., v. 2, n. 1, p. 27-39, 2007b.; SOUZA-CONCEIÇÃO et al., 2013SOUZA-CONCEIÇÃO, J. M.; SPACH, H. L.; BORDIN, D.; FRISANCO, D.; COSTA, M. D. P. The role of estuarine beaches as habitats for fishes in a Brazilian subtropical environment. Neotrop. Biol. and Cons., v. 8, n. 3, p. 121-131, 2013.; PEREIRA et al., 2014PEREIRA, H. H.; NEVES, L. M.; COSTA, M. R.; ARAÚJO, F. G. Fish assemblage structure on sandy beaches with different anthropogenic influences and proximity of spawning grounds. Mar. Ecol., p. 1-12, 2014.), they were only sampled in the larval stage in the study area. Araújo and Santos (1999)ARAÚJO, F. G.; SANTOS, A. C. A. Distribution and recruitment of Mojarras (Perciformes, Gerreidae) in the continental margin of Sepetiba Bay, Brazil. Bull. Mar. Sci., v. 65, n. 2, p. 431-439, 1999. found that juvenile gerreids prefer less-turbid regions, with mud and moderate organic matter substrates, while GODEFROID et al. (1999GODEFROID, R. S; HOFSTAETTER, M.; SPACH, H. L. Larval fish in the surf zone of Pontal do Sul beach, Pontal do Parana, Parana, Brazil. Rev. Bras. Zool., v. 16, n. 4, p. 1005-1011, 1999.; 2001GODEFROID, R. S; SANTOS, C.; HOFSTAETTER, M.; SPACH, H. L. Occurrence of Larvae and Juveniles of Eucinostomus argenteus, Eucinostomus gula, Menticirrhus americanus, Menticirrhus littoralis, Umbrina coroides and Micropogonias furnieri at Pontal do Sul beach, Paraná. Braz. Arch. Biol. Technol., v 44, n 4, p. 411-418, 2001.) found 98% of gerreids in the larval stage, corroborating the findings of this study.

The present study highlights the importance of the sandy beaches for juvenile fish, whether as a migration route or as a growth area, especially in spring and summer when most juveniles recruit. Unfortunately, this period is the one with the greatest tourism impact. PEREIRA et al. (2014)PEREIRA, H. H.; NEVES, L. M.; COSTA, M. R.; ARAÚJO, F. G. Fish assemblage structure on sandy beaches with different anthropogenic influences and proximity of spawning grounds. Mar. Ecol., p. 1-12, 2014. indicated that less anthropogenic disturbance on the beach results in greater fish richness and abundance. important, emphasizing the necessity of coastal habitat preservation for better fishery management.

ACKNOWLEDGEMENTS

The authors would like to thank all the IOUSP volunteers and employees involved in the fieldwork and fish identification. We also thank CNPq, which has granted the author's postgraduate scholarship, Dr. Carlos A. Assis for reviewing the manuscript and Dr. Jefferson T. Turner for the English editing.

REFERENCES

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    Apr-Jun 2015
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