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Temporal dynamics of a fish community in the lower portion of a tidal creek, Pando sub-estuarine system, Uruguay

Dinâmica temporal de uma comunidade de peixes na parte baixa de um arroio costeiro, sistema subestuarino Pando, Uruguai

ABSTRACT

Estuaries are highly dynamic ecosystems subjected to variability of their fish communities over different time scales. The nearshore fish community of the lower Pando estuary, a temperate sub-system of the Río de la Plata estuary, was sampled from May 2002 to June 2003. A total of 2,165 fishes, represented by 16 species were caught by seine netting. Captures were dominated by juveniles (>90%), as well as by the sciaenid Micropogonias furnieri (Desmarest, 1823) (82.8%). The fish community showed high seasonal variability, with the greatest diversity and biomass in summer and spring and the highest species richness during summer. Lowest values of all community parameters occurred in winter and autumn, seasons that presented the highest similarity in fish composition. Number of species was correlated with water temperature and salinity. The ichthyofaunal composition showed significant diel differences in summer and spring. Diel changes were observed in the density of M. furnieri and Odontesthes argentinensis (Valenciennes, 1835), occurring mainly during the day, and of Mugil liza Valenciennes, 1836, Parapimelodus valenciennis (Lütken, 1874) and Brevoortia aurea (Spix & Agassiz, 1829), caught mostly during the night. Temporal variability was attributed to environmental fluctuations, life cycle of species as well as to feeding patterns and small-scale displacements. Presented findings in the Pando sub-estuary denote similar juvenile use and seasonal patterns to those found in estuaries. Further studies in the nursery function and juvenile dynamics over the year are recommended in order to better understand the ecological role of sub-estuaries.

KEYWORDS
Ichthyofauna; community parameters; seasonal variability; diel variability; sub-estuary

RESUMO

Os estuários são ecossistemas dinâmicos que apresentam variabilidade nas suas comunidades de peixes em diferentes escalas de tempo. A comunidade de peixes costeiros do baixo estuário do Pando, um subsistema temperado do estuário do Río de la Plata, foi amostrada entre maio de 2002 e junho de 2003. Um total de 2.165 peixes, representados por 16 espécies, foi documentado com a pesca de arrasto. As capturas foram dominadas pelos jovens (>90%), assim como pelo sciaenídeo Micropogonias furnieri (Desmarest, 1823) (82,8%). A comunidade de peixes apresentou uma grande mudança sazonal, com a máxima diversidade e biomassa no verão e primavera, e a máxima riqueza de espécies durante o verão. Os menores valores de todos os parâmetros comunitários ocorreram no inverno e outono, estações com a maior similaridade na composição da ictiofauna. O número de espécies foi correlacionado com a temperatura de água e salinidade. A composição da ictiofauna apresentou mudanças significativas diárias no verão e primavera. Verificou-se uma variabilidade diária na densidade da M. furnieri e Odontesthes argentinensis (Valenciennes, 1835), ocorrendo principalmente durante o dia, e de Mugil liza Valenciennes, 1836, Parapimelodus valenciennis (Lütken, 1874) e Brevoortia aurea (Spix & Agassiz, 1829), observadas principalmente durante à noite. A variabilidade temporal foi atribuída a interação com o ambiente, ciclo de vida das espécies assim como a atividade alimentar e movimentos de pequena escala. Resultados no subestuário Pando denotam um uso de juvenis e padrões sazonais semelhante aos dos estuários. Mais pesquisas no papel das áreas de berçário e dinâmicas juvenis ao longo do ano são recomendadas para compreender melhor o papel ecológico dos subestuários.

PALAVRAS-CHAVE
Ictiofauna; parâmetros da comunidade; variabilidade sazonal; variabilidade diária; subestuário

Estuaries have been widely recognized as essential ecosystems for the development of key functions in the life cycle of fish species. Estuaries are highly productive environments, acting as nursery areas, feeding grounds and temporal habitats for a wide range of fish species (Day et al., 2013Day, J. W.; Crump, Jr. B. C.; Kemp, W. M. & Yáñez-Arancibia, A. 2013. Estuarine Ecology. Hoboken, Wiley-Blackwell, John Wiley & Sons. 500p.). Due to high dynamism, estuarine waters have been subjected to many studies quantifying the temporal variability of biotic and abiotic parameters (Akin et al., 2005Akin, S.; Buhan, E.; Winemiller, K. O. & Yilmaz, H. 2005. Fish assemblage structure of Koycegiz lagoon-estuary, Turkey: Spatial and temporal distribution patterns in relation to environmental variation. Estuarine, Coastal and Shelf Science 64:671-684.; Barletta et al., 2008Barletta, M.; Amaral, C. S.; Correa, M. F. M.; Guebert, F.; Dantas, D. V.; Lorenzi, L. & Saint-Paul, U. 2008. Factors affecting seasonal variations in demersal fish assemblages at an ecocline in a tropical-subtropical estuary. Journal of Fish Biology 73:1314-1336.). Therefore, a number of temporal scales, including seasonal and diel scales, have been suggested (Hoeksema & Potter, 2006Hoeksema, S. D. & Potter, I. C. 2006. Diel, seasonal, regional and annual variations in the characteristics of the ichthyofauna of the upper reaches of a large Australian microtidal estuary. Estuarine, Coastal and Shelf Science 67:503-520.).

In the seasonal cycle, recruitment, migration and bio-environmental interaction are some examples of biological processes taking place in estuaries (Idelberger & Greenwood, 2005Idelberger, C. F. & Greenwood, M. F. D. 2005. Seasonal variation in fish assemblages within the estuarine portions of the Myakka and Peace rivers, southwest Florida. Gulf of Mexico Science 2:224-240.; Barletta et al., 2008Barletta, M.; Amaral, C. S.; Correa, M. F. M.; Guebert, F.; Dantas, D. V.; Lorenzi, L. & Saint-Paul, U. 2008. Factors affecting seasonal variations in demersal fish assemblages at an ecocline in a tropical-subtropical estuary. Journal of Fish Biology 73:1314-1336.). Changes in density, biomass and number of species of the estuarine fish assemblages in temperate estuaries are often reported (Hagan & Able, 2003Hagan, S. M. & Able, K. W. 2003. Seasonal changes of the pelagic fish assemblage in a temperate estuary. Estuarine, Coastal and Shelf Science 56:15-29.; Barletta et al., 2008Barletta, M.; Amaral, C. S.; Correa, M. F. M.; Guebert, F.; Dantas, D. V.; Lorenzi, L. & Saint-Paul, U. 2008. Factors affecting seasonal variations in demersal fish assemblages at an ecocline in a tropical-subtropical estuary. Journal of Fish Biology 73:1314-1336.). Environmental variability such as salinity and temperature fluctuations, and timing of both reproduction and life history characteristics, have been the most commonly invoked drivers of the observed patterns (Hagan & Able, 2003Hagan, S. M. & Able, K. W. 2003. Seasonal changes of the pelagic fish assemblage in a temperate estuary. Estuarine, Coastal and Shelf Science 56:15-29.; Simier et al., 2006Simier, M.; Laurent, C.; Ecoutin, J. & Albaret, J. 2006. The Gambia River estuary: a reference point for estuarine fish assemblages studies in West Africa. Estuarine, Coastal and Shelf Science 69:615-628.).

Throughout diel temporal scales, fish dynamics are closely related to feeding patterns, avoidance of potential predators or adverse physicochemical conditions and use of shelter habitats (Oliveira-Neto et al., 2008Oliveira-Neto, J. F.; Spach, H. L.; Schwarz-Junior, R. & Pichler, H. A. 2008. Diel variation in fish assemblages in tidal creeks in southern Brazil. Brazilian Journal of Biology 68(1):37-43.; Castillo-Rivera et al., 2010Castillo-Rivera, M.; Zárate-Hernández, R.; Ortiz-Burgos, S. & Zavala-Hurtado, J. 2010. Diel and seasonal variability in the fish community structure of a mud-bottom estuarine habitat in the Gulf of Mexico. Marine Ecology 31(4):633-642.; Becker et al., 2011Becker, A.; Cowley, P. D.; Whitfield, A. K.; Jarnegren, J. & Naesje, T. F. 2011. Diel fish movements in the littoral zone of a temporarily closed South African estuary. Journal of Experimental Marine Biology and Ecology 406:63-70.). Among the proposed factors controlling these interactions, photoperiod has been suggested as one of the most important (Gaelzer & Zalmon, 2008Gaelzer, L. R. & Zalmon, I. R. 2008. Diel Variation of fish community in sandy beaches of southeastern Brazil. Brazilian Journal of Oceanography 56:23-39.). Light levels provide an easily quantifiable assessment of risk from predators, linking diel movements to feeding ecology and predator avoidance of fish species. Thus, species can respond to diel variation by timing activity levels with the diel period (Clark et al., 2003Clark, K. L.; Ruiz, G. M. & Hines, A. H. 2003. Diel variation in predator abundance, predation risk and prey distribution in shallow-water estuarine habitats. Journal of Experimental Marine Biology and Ecology 287:37-55.).

The Río de la Plata (RdlP) system constitutes one of the largest estuaries in the world. The marginal Uruguayan coast of the RdlP has been suggested as a nursery fish habitat (Retta et al., 2006Retta, S.; Martinez, G. & Errea, A. 2006. Área de cría de peces en la costa uruguaya. In: Menafra, R.; Rodriguez-Gallego, L.; Scarabino, F. & Conde, D. eds. Bases para la conservación y el manejo de la costa uruguaya. Montevideo, Vida Silvestre, p. 221-218.). Along this coast a series of sub-estuarine creeks flow into the RdlP, among which is located the Pando sub-estuarine system. Previous studies conducted in this system described the temporal distribution of fish species, highlighting the ecological role of the Pando sub-estuary as a nursery ground for juvenile fish, mainly for the species Micropogonias furnieri (Desmarest, 1823) (Acuña et al., 2010Acuña, A. P.; Passadore, C. & Gimenez, L. 2010. Fish assemblage in a temperate estuary on the Uruguay coast: seasonal variation and environmental influence. Brazilian Journal of Oceanography 58(4):299-314.). Acuña et al. (2010)Acuña, A. P.; Passadore, C. & Gimenez, L. 2010. Fish assemblage in a temperate estuary on the Uruguay coast: seasonal variation and environmental influence. Brazilian Journal of Oceanography 58(4):299-314. suggested a correlation between the fish abundance and temperature, as well as advised on the role of salinity over the functional structure and juvenile use of the area.

To date, little is known about the temporal dynamics of fish communities in sub-estuaries apart from the general trend found in estuaries. In this sense, the purpose of the present study was to compliment the seasonal analysis undertaken by Acuña et al. (2010Acuña, A. P.; Passadore, C. & Gimenez, L. 2010. Fish assemblage in a temperate estuary on the Uruguay coast: seasonal variation and environmental influence. Brazilian Journal of Oceanography 58(4):299-314.), and to determine the diel variability of the fish community in the Pando sub-estuary. Therefore, the aim was to determine the seasonal and diel composition of the fish community, analyse the seasonal and diel variability and relate these patters to the environmental fluctuations. No-differences in the fish composition, abundance, species richness or diversity were proposed between seasons or diel periods.

MATERIALS AND METHODS

The Pando tidal creek system (34°47'S, 55°52'W) is a small temperate sub-estuary influenced by tidal waters of the RdlP (Acha et al., 2008Acha, E. M.; Mianzan, H.; Guerrero, R.; Carreto, J.; Giberto, D.; Montoya, N. & Carignan, M. 2008. An overview of physical and ecological processes in the Río de la Plata estuary. Continental Shelf Research 28:1579-1588.) (Fig. 1). No data exist on astronomical tides for Pando estuary, but the adjacent area of the RdlP presents small tidal amplitude (0.3 m) (Mtop-Pnud, 1979Mtop-Pnud, 1979. Proyecto sobre conservación y mejora de playas (URU. 73007). Montevideo, Ministerio de Transporte y Obras Públicas, UNESCO. 593p.). The Pando estuary covers a drainage basin of 973 km² and has an average flow of 10.9 m³/s (Cayssials et al., 2000Cayssials, R.; Hernández, J.; Cantón, V.; Fernández, V.; Laborde, J. L. & Collazo, D. 2000. Caracterización del medio físico. In: Laborde, J. L.; Perdomo, A. & Gómez-Erache, M. eds. Diagnóstico ambiental y socio-demográfico de la zona costera uruguaya del Río de la Plata. Montevideo, Ecoplata, p. 14-73.).

Fig. 1
Study area in the lower Pando sub-estuary, Uruguay. Sampling location is indicated by a black circle.

The study was carried out between May 2002 and June 2003 (except in May 2003), during the afternoon. Once a month fish was collected at three replicate sites in nearshore waters by seine net (12 m long, 2 m high, 12 mm knot-to-knot), with two 25 m long ropes joined to each end of the net. The net was laid parallel to the shore and then hauled onto the beach, in order to sample fish to a depth of 1.5 m (swept area of 300 m2). Additionally, during August 2002 (winter), December 2002 (spring), February 2003 (summer) and June 2003 (autumn), sampling was designed to obtain fish data throughout one 24-hour period, with 18 hauls divided between light and dark hours. Simultaneously, the water temperature and salinity were measured using a multi-parameter device.

Fish were identified to species according to Ringuelet et al., 1967Ringuelet, R. A.; Aramburu, R. H. & De Aramburu, A. A. 1967. Los peces argentinos de agua dulce. La Plata, Comisión de Investigación Científica. 602p.; Figueiredo & Menezes (1978Figueiredo, J. L. & Menezes, N. A. 1978. Manual de peixes marinhos do sudeste do Brasil. II. Teleostei (1). São Paulo, Museu de Zoologia da Universidade de São Paulo. 110p.; 1980Figueiredo, J. L. & Menezes, N. A. 1980. Manual de peixes marinhos do sudeste do Brasil. III. Teleostei (2). São Paulo, Museu de Zoologia da Universidade de São Paulo . 98p.), Menezes & Figueiredo (1980)Menezes, N. A. & Figueiredo, J. L. 1980. Manual de peixes marinhos do sudeste do Brasil. IV. Teleostei (3). São Paulo, Museu de Zoologia da Universidade de São Paulo . 96p., Menni et al. (1984Menni, R. C.; Ringuelet, R. A. & Aramburu, R. H. 1984. Peces marinos de la Argentina y Uruguay. Buenos Aires, Editorial Hemisferio Sur. 359p.), Menezes & Figueiredo (1985)Menezes, N. A. & Figueiredo, J. L. 1985. Manual de peixes marinhos do sudeste do Brasil. V. Teleostei (4). São Paulo, Museu de Zoologia da Universidade de São Paulo . 96p., Figueiredo & Menezes (2000)Figueiredo, J. L. & Menezes, N. A. 2000. Manual de peixes marinhos do sudeste do Brasil. VI. Teleostei (5). São Paulo, Museu de Zoología da Universidade de São Paulo. 116p. and Dyer (2006Dyer, B. S. H. 2006. Systematic revision of the South American silversides (Teleostei, Atheriniformes). Biocell 30(1):69-88.), counted, measured to the nearest 1 mm and weighed to the nearest 0.1 g.

Fish community parameters (number of fish, species richness, diversity, through Shannon-Wiener index, and biomass) were compared between seasons and day periods (day and night). Assumptions of normality and homogeneity of variance were analysed by Shapiro Wilk's test (Shapiro & Wilk, 1965Shapiro, S. S. & Wilk, M. B. 1965. An analysis of variance test for normality (Complete samples). Biometrika 52:591-611.) and Levene's test (based on the averages), respectively. When necessary, data were transformed to Log (n) or Log (n+1). Parametric analysis of variance (ANOVA) or non-parametric Kruskal-Wallis was used depending on the fulfilment of the assumptions. A post hoc Tukey's Test or Mann-Whitney was used to test for multiple comparisons. To test whether the ichthyofaunal composition differed significantly between seasons or day period, a similarity matrix was subjected to one-way analysis of similarity (ANOSIM) (Clarke, 1993Clarke, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18:117-143.) using the PRIMER 6 multivariate statistics package. The Bray Curtis similarity matrix was constructed employing log transformed (n+1) densities of fish species. The R-statistic values determined by ANOSIM for significant comparisons were used to ascertain the degree to which a priori groups of samples were dissimilar (Clarke, 1993Clarke, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18:117-143.). R-statistic values approaching unity demonstrate that the compositions of the samples in each group are very different, while those close to zero show that they are very similar. To analyse the temporal contribution of each species to its annual total catch, the percentage contribution of the main fish species in each season was plotted. Spearman rank correlation coefficients (ρ) were used to determine the extent to which fish distributions were correlated with abiotic variables. A significance level of α = 0.05 was established (Sokal & Rohlf, 1969Sokal, R. R. & Rohlf, J. F. 1969. Biometria. New York, Freeman W.H. and Company. 832p.).

RESULTS

Mean seasonal water temperature and salinity values ranged from 11.1° C to 24.4° C and from 2.4 to 10.9, respectively (Tab. I). Significant differences were found between seasons for both variables (Kruskal-Wallis, p < 0.001). Maximum temperature and salinity values were registered during summer, while minimum temperature and salinity values occurred during autumn and winter, respectively (Tab. I). Diel variability only showed significant differences in summer, with the highest salinity values occurring during day (ANOVA, p < 0.05) (Tab. I).

Tab. I
Environmental data measured from May 2002 to June 2003 in the lower Pando sub-estuary, Uruguay. Data is expressed as mean value ± standard deviation. * = no data register.

A total of 2,165 individuals, belonging to 16 species and eleven families and weighing 53.39 kg were caught by seine netting during monthly and diel sampling (Tab. II). Captured fish were predominately juveniles (>90%). Micropogonias furnieri was the most abundant species, both in number of individuals (82.8%) and biomass (38.1%), caught in all sampling periods and represented by more than 99% of juveniles. Other representative species in terms of number of individuals were Mugil liza Valenciennes, 1836 (7.6%) and Odontesthes argentinensis (Valenciennes, 1835) (2%). Cyprinus carpio Linnaeus, 1758 (25.7%) and Paralichthys orbignyanus (Valenciennes, 1839) (15.9%) were also abundant in terms of biomass, representing the largest individuals in the fish community (Tab. II). In terms of the seasonal variability of the most abundant species, M. furnieri was the only species with a constant occurrence throughout the year (Fig. 2). Mugil liza, Parapimelodus valenciennis (Lütken, 1874) and P. orbignyanus were most abundant during spring, O. argentinensis and Brevoortia aurea (Spix & Agassiz, 1829) during summer and Platanichthys platana (Regan, 1917) during winter (Fig. 2).

Tab. II
Taxonomic, abundance and morphometric data of fish community caught by seine netting from May 2002 to June 2003 in the lower Pando sub-estuary, Uruguay (R, rankings by abundance; N, numbers; g, grams; %, percentage contributions to total catch; LR, length range; ML, mean length; % OF, percentage of occurrence frequency).

Fig. 2
Seasonal changes in percentage contribution of the most abundant species caught by seine netting from May 2002 to June 2003 in the lower Pando sub-estuary, Uruguay.

Seasonal differences were detected in biomass, species richness, diversity and fish composition of the community (Kruskal-Wallis, p < 0.001; ANOSIM, p = 0.001, except for winter and autumn with p < 0.05), except for the number of individuals (Kruskal-Wallis, p > 0.05). According to comparisons of the community parameters, summer and spring could be classified as periods with the greatest diversity and biomass of the fish community, compared to winter and autumn (Fig. 3; Tab. III). Maximum average values of fish species richness (4/300 m2) and diversity (0.72/300 m2) were found during summer, while highest average values of biomass occurred in spring (4.53 kg/1000 m2) (Fig. 3). All parameters presented minimum average values during winter and autumn (Fig. 3). Highest similarity in fish composition were found between winter-autumn (ANOSIM, R = 0.098), followed by summer-autumn (ANOSIM, R = 0.312), summer-winter (ANOSIM, R = 0.389) and summer-spring (ANOSIM, R = 0.432). A significant correlation was detected between number of species and both water temperature (Spearman, ρ = 0.54, p < 0.05) and salinity (Spearman, ρ = 0.51, p = 0.05).

Fig. 3
Seasonal variability of fish catch data in terms of mean (± SD) biomass (biomass/ 1000 m2), number of fish (fish number/ 1000 m2), species richness (species/300 m2) and diversity (diversity value/300 m2) from May 2002 to June 2003 in the lower Pando sub-estuary, Uruguay.

Tab. III
Significance levels (Mann-Whitney test) obtained from comparing fish community parameters between seasons of the year from May 2002 to June 2003 in the lower Pando sub-estuary, Uruguay (* = p < 0.05; ** = p < 0.01; *** = p < 0.001; ns, no significant difference).

Analysis of diel variability performed seasonally only showed significant differences in density and biomass during winter (ANOVA, p < 0.05), with highest average values during the day (86 individuals/1000 m2; 1,008.6 g/1000 m2) (Fig. 4). Ichthyofaunal composition differed significantly between day and night in summer and spring (ANOSIM, p < 0.01). Diel patterns in the fish composition were largely attributed to M. furnieri, M. liza, O. argentinensis, P. valenciennis and B. aurea, as well as to the occurrence of occasional species (Tab. IV). Micropogonias furnieri showed greater average density (77 individuals/1000 m2) (Kruskal-Wallis, p < 0.05) and biomass (436.5 g/1000 m2) (Kruskal-Wallis, p < 0.001) during the day in winter (Tab. IV). Mugil liza, P. valenciennis and B. aurea were mainly caught at night, during autumn (five individuals/1000m2) (Kruskal-Wallis, p < 0.05), spring (nine individuals/ 1000 m2) (Kruskal-Wallis, p < 0.01) and summer (six individuals/ 1000 m2) (Kruskal-Wallis, p < 0.01), respectively (Tab. IV). Odontesthes argentinensis was more abundant in the day (eight individuals/ 1000 m2) (Kruskal-Wallis, p < 0.05) in summer (Tab. IV). The higher density of O. argentinensis during the day was correlated with the salinity values (Spearman, ρ = 1, p < 0.05) (Fig. 5).

Fig. 4
Diel variability of the fish community in terms of density and biomass (mean value ± SD) in different seasons (from left to right: winter, spring, summer and autumn) in the lower Pando sub-estuary, Uruguay.

Tab. IV
Diel fish catch differences by season of the year caught by seine netting from May 2002 to June 2003 in the lower Pando sub-estuary, Uruguay (D, day; N, night). Data is expressed in mean density (N) (individuals/ 1000 m2), mean biomass (g) (g/1000 m2).

Fig. 5
Relationship between number of fish (mean fish number/1000 m2) of species Odontesthes argentinensis (Valenciennes, 1835) and salinity during summer in the lower Pando sub-estuary, Uruguay.

DISCUSSION

Over the study period the lower portion of the Pando sub-estuary presented a low number of fish species, compared to tropical estuaries (Arceo-Carranza & Vega-Cendejas, 2009Arceo-Carranza, D. & Vega-Cendejas, M. E. 2009. Spatial and temporal characterization of fish assemblages in a tropical coastal system influenced by freshwater inputs: northwestern Yucatan peninsula. Revista de Biología Tropical (International Journal of Tropical Biology and Conservation) 57(1-2):89-103.; Zárate-Hernández et al., 2012Zárate-Hernández, R.; Castillo-Rivera, M.; Sanvicente-Añorve, L. & Ortiz-Burgos, S. 2012. Spatial, diel, and seasonal changes in the fish community structure of a Mexican tropical estuary. Ciencias Marinas 38(4):665-676.). The species richness and fish composition was consistent with what has been found in adjacent sub-estuarine systems along the Uruguayan coast (Gurdek et al., 2016Gurdek, R.; De La Rosa, A.; Corrales, D.; Canavese, R.; Gutierre, J. M.; Stebniki, S.; Muñoz, N.; Severi, V. & Acuña-Plavan, A. 2016. Estuarine use and composition of fish species in the Solís Grande sub-estuary, Uruguay. Pan-American Journal of Aquatic Sciences 11(1):82-86.; Acuña et al., in pressAcuña, A. P.; Gurdek, R.; Muñoz, N.; Gutierrez, J. M.; Spósito, M.; Correa, P. & Caride, A. Seasonal composition, abundance and biomass of the subestuarine fish assemblage in Solís Chico (Río de la Plata estuary, Uruguay). Brazilian Journal of Biology. In press. http://dx.doi.org/10.1590/1519-6984.02216
https://doi.org/10.1590/1519-6984.02216...
). Similar results were found in temperate estuarine systems by James et al. (2008)James, N. C.; Whitfield, A. K. & Cowley, P. D. 2008. Long-term stability of the fish assemblages in a warm-temperate South African estuary. Estuarine, Coastal and Shelf Science 76:723-738., Loebmann et al. (2008Loebmann, D.; Vieira, J. P.; Bemvenuti, M. A.; Astarloa, J. M. D.; Cousseau, M. B. & Figueroa, D. 2008. Composição e abundância da ictiofauna de duas lagunas costeiras da América do Sul Austral: lagoa do Peixe (31°S; 51°W), Brasil e laguna Mar Chiquita (37°S; 57°W), Argentina. Neotropical Biology and Conservation 3:28-33.), Cardoso et al. (2011)Cardoso, I.; Franca, S.; Pais, M. P.; Henriques, S.; Fonseca, L. C. & Cabral, H. N. 2011. Fish assemblages of small estuaries of the Portuguese coast: A functional approach. Estuarine, Coastal and Shelf Science 93:40-46. and Bruno et al. (2013Bruno, D. O.; Barbini, S. A.; Astarloa, J. M. D. & Martos, P. 2013. Fish abundance and distribution patterns related to environmental factors in a choked temperate coastal lagoon (Argentina). Brazilian Journal of Oceanography 61:43-53.). However, the collected number of species could be low in comparison to other temperate estuaries (Potter et al., 1990Potter, I. C.; Beckley, L. E.; Whitfield, A. K. & Lenanton, R. C. J. 1990. Comparisons between the roles played by estuaries in the life cycles of fishes in temperate Western Australia and Southern Africa. Environmental Biology of Fishes 28:143-178.). A relatively low number of species can be linked to properties such as latitude (i.e., temperate latitude), estuary area (i.e., small size) and diversity of habitats (i.e., poor habitat diversity) (Franca et al., 2011Franca, S.; Costa, M. J. & Cabral, H. N. 2011. Inter- and intra-estuarine fish assemblage variability patterns along the Portuguese coast. Estuarine, Coastal and Shelf Science 91:262-271.; Pasquaud et al., 2015Pasquaud, S.; Vasconcelos, R. P.; Franca, S.; Henriques, S.; Costa, M. J. & Cabral, H. N. 2015. Worldwide patterns of fish biodiversity in estuaries: effect of global vs. local factors. Estuarine, Coastal and Shelf Science 154:122-128.). Also, low salinity values can mean a natural disturbance imposed in an estuary to the fish assemblage (Albaret et al., 2004Albaret, J. J.; Simier, M.; Darboe, F. S.; Ecoutin, J. M.; Raffry, J. & de Morais, L. T. 2004. Fish diversity and distribution in the Gambia estuary, West Africa, in relation to environmental variables. Aquatic Living Resources 17:35-46.). During the sampling period the Pando waters were influenced by El Niño Southern Oscillation (Bidegain et al., 2005Bidegain, M.; Caffera, F. R. M.; Blixen, F.; Pshennikov, V. J.; Lagomarsino, J.; Forbes, E. A. & Nagy, G. J. 2005. Tendencias climáticas, hidrológicas y oceanográficas en el Río de la Plata y costa uruguaya. In: Barros, V.; Menéndez, A. & Nagy, G. eds. El cambio climático en el Río de la Plata. Buenos Aires, CIM, CONICET, p. 137-143.), which caused salinity values to decrease. Contrasting environmental conditions are expected to occur in the Pando compared to other estuaries, since the Pando sub-estuary is connected to an estuary (i.e., RdlP) rather than to oceanic waters.

Fish assemblage of the study system was dominated by juvenile individuals, which is a common pattern found in estuaries around the world due to the ecological functions they provide, particularly for postlarvae and juveniles (Potter & Hyndes, 1999Potter, I. C. & Hyndes, G. A. 1999. Characteristics of the ichthyofaunas of southwestern Australian estuaries, including comparisions with holarctic estuaries and estuaries elsewhere in temperate Australia: A review. Australian Journal of Ecology 24:395-421.; McLusky & Elliott, 2004McLusky, D. S. & Elliott, M. 2004. The estuarine ecosystem: ecology, threats and management. New York, Oxford University Press. 214p.). Another common feature observed was the dominance of a few fish species, mainly by the sciaenid M. furnieri in juvenile stages. Micropogonias furnieri is a widely distributed species along the western Atlantic coast, being the most abundant species in the estuarine RdlP (García et al., 2010García, M. L.; Jaureguizar, A. J. & Protogino, L. C. 2010. From fresh water to the slope: fish community ecology in the Río de la Plata and the sea beyond. Latin American Journal of Aquatic Research 38(1):81-94.), where the species spawns (Macchi et al., 1996Macchi, G. J.; Acha, M. E. & Lasta, C. A. 1996. Desove y fecundidad de la corvina rubia Micropogonias furnieri Desmarest, 1823 del estuario del Río de la Plata, Argentina. Boletín Instituto Español de Oceanografía 12(2):99-113.). These findings denote the importance of the Pando sub-estuarine system as a nursery ground in the life cycle of fish species that use the RdlP as a spawning ground (Acuña et al., 2010Acuña, A. P.; Passadore, C. & Gimenez, L. 2010. Fish assemblage in a temperate estuary on the Uruguay coast: seasonal variation and environmental influence. Brazilian Journal of Oceanography 58(4):299-314.).

On the other hand, largest individuals such as P. orbignyanus reached the maximum size of the species and were captured by the end of winter. Maximum size individuals of the species also occurred in an adjacent sub-estuarine system, Solís Grande, in the same period (Rodrigo Gurdek, pers. observ.). It is suggested a seasonal movement of the largest individuals of P. orbignyanus from the RdlP into the sub-estuaries, which could be related to the breeding season. On the other hand, the register of C. carpio in the lower sub-estuary denotes the extension of the distribution of this freshwater invasive species in the Pando system, possibly regulated by river discharge. As well, the same species was captured in the Solís Grande sub-estuary under minimum salinity values (around 0). Individuals of C. carpio were also registered in the Solís Grande in salinities values of around 20, suggesting a higher salinity tolerance range than expected (Rodrigo Gurdek, pers. observ.).

Environmental characteristics constitute a main factor in structuring fish associations (Thiel et al., 1995Thiel, R.; Sepúlveda, A.; Kafemann, R. & Nellen, W. 1995. Environmental factors as forces structuring the fish community of the Elbe Estuary. Journal of Fish Biology 46:47-69.; Whitfield, 1999Whitfield, A. K. 1999. Ichthyofaunal assemblages in estuaries: A South African case study. Reviews in Fish Biology and Fisheries 9:151-186.; Selleslagh & Amara, 2008Selleslagh, J. & Amara, R. 2008. Environmental factors structuring fish composition and assemblages in a small macrotidal estuary (eastern English Channel). Estuarine, Coastal and Shelf Science 79:507-517.). In the Pando estuary, highest diversity and species richness values occurred when water temperature and salinity reached their maximums (i.e., summer followed by spring). Additionally, fish composition was more similar during the cold seasons (i.e., winter and autumn) than between summer and the rest of the seasons. Previous studies in the Pando estuary indicated the significant role of temperature and salinity in structuring the use of habitat by juveniles, suggesting a correlation between temperature and estuarine fish abundance, and between salinity and marine migrants abundance (Acuña et al., 2010Acuña, A. P.; Passadore, C. & Gimenez, L. 2010. Fish assemblage in a temperate estuary on the Uruguay coast: seasonal variation and environmental influence. Brazilian Journal of Oceanography 58(4):299-314.). Jaureguizar et al. (2004Jaureguizar, A. J.; Menni, R.; Guerrero, R. & Lasta, C. 2004. Environmental factors structuring fish communities of the Río de la Plata estuary. Fisheries Research 66:195-211.) suggested temperature as the abiotic parameter with the strongest influence on seasonal structure of fish assemblages in the RdlP. Seasonal and reproductive movements, and relative abundance of fish species within the fish assemblages in the RdlP populations could be the result of salinity and temperature fluctuations (Jaureguizar et al., 2004Jaureguizar, A. J.; Menni, R.; Guerrero, R. & Lasta, C. 2004. Environmental factors structuring fish communities of the Río de la Plata estuary. Fisheries Research 66:195-211.). Similar results were found by Hoeksema & Potter (2006Hoeksema, S. D. & Potter, I. C. 2006. Diel, seasonal, regional and annual variations in the characteristics of the ichthyofauna of the upper reaches of a large Australian microtidal estuary. Estuarine, Coastal and Shelf Science 67:503-520.) in a temperate Australian estuary, describing the maximum number and abundance of fish species during summer and the minimum during winter. These authors demonstrated that seasonal differences in fish composition were greater between opposite seasons, reinforcing the idea of considering both environmental variability and life cycles of fish species when addressing temporal variability in estuarine environments.

Greenwood et al. (2007Greenwood, M. F. D.; Matheson, Jr. R. E.; McMichael, Jr. R. H. & MacDonald, T. C. 2007. Community structure of shoreline nekton in the portion of the Alafia river, Florida: Differences along a salinity gradient and inflow-related changes. Estuarine, Coastal and Shelf Science 74:223-238.) observed regular seasonal changes in the fish community structure in the lower portion of an estuary in the United States. Authors attributed those patterns to the biological cycle of transient species (i.e., spawning and migration patterns). In the Pando sub-estuary, seasonal movements performed by the most numerous fish species (including reproduction pulses, since many individuals were juveniles in the first part of their life cycle), along with occurrence of rare species, are suggested as the main factors. On the other hand, the highest and constant occurrence over the year of the dominant species M. furnieri would explain the lack of differences in number of individuals between seasons.

The fish abundance, number of species and diversity did not differ substantially between day and night in any season, except for winter, with higher abundance values in the day. These results were consistent with those found by Pessanha & Araújo (2003Pessanha, A. L. M. & Araújo, F. G. 2003. Spatial, temporal and diel variations of fish assemblages at two sandy beaches in the Sepetiba bay, Rio de Janeiro, Brazil. Estuarine, Coastal and Shelf Science 57:817-828.) and Ribeiro et al. (2006Ribeiro, J.; Bentes, L.; Coelho, R.; Gonçalves, J. M. S.; Lino, P. G.; Monteiro, P. & Erzini, K. 2006. Seasonal, tidal and diurnal changes in fish assemblages in the Ria Formosa lagoon (Portugal). Estuarine, Coastal and Shelf Science 67:461-474.) in estuarine systems from Brazil and Portugal. Pessanha & Araújo (2003)Pessanha, A. L. M. & Araújo, F. G. 2003. Spatial, temporal and diel variations of fish assemblages at two sandy beaches in the Sepetiba bay, Rio de Janeiro, Brazil. Estuarine, Coastal and Shelf Science 57:817-828. stated that changes in assemblage structure were caused by shifts in abundance of particular species. In the present study, diel patterns in the fish community density and biomass were largely attributed to M. furnieri occurrence. Clark et al. (2003Clark, K. L.; Ruiz, G. M. & Hines, A. H. 2003. Diel variation in predator abundance, predation risk and prey distribution in shallow-water estuarine habitats. Journal of Experimental Marine Biology and Ecology 287:37-55.) in a temperate sub-estuary from the United States found higher number of a related species, Micropogonias undulatus (Linnaeus, 1766), during the day. This variability was associated to feeding patterns of the species, which depended on the occurrence of its preys. In the Pando sub-estuary, an absence of a diel feeding cycle has been suggested for the species over the year, however diet analysis in winter determined that full stomachs were predominant during daytime (Ruben Canavese, pers. comm.).

In addition to M. furnieri, specific diel changes were registered for M. liza, P. valenciennis and B. aurea showing higher abundances at night, which could be related to feeding activity and predator avoidance (Becker et al., 2011Becker, A.; Cowley, P. D.; Whitfield, A. K.; Jarnegren, J. & Naesje, T. F. 2011. Diel fish movements in the littoral zone of a temporarily closed South African estuary. Journal of Experimental Marine Biology and Ecology 406:63-70.). At the diel scale, Methven et al. (2001Methven, D. A.; Haedrich, R. L. & Rose, G. A. 2001. The fish assemblage of a Newfoundland estuary: diel, monthly and annual variation. Estuarine, Coastal and Shelf Science 52:669-687.) in a Newfoundland estuary observed both, species that showed no significant difference between day and night, and species caught primarily at night, suggesting an onshore movement of these species during night. Mugilids tended to be nocturnal in estuarine habitats of Brazil (Pessanha & Araújo, 2003Pessanha, A. L. M. & Araújo, F. G. 2003. Spatial, temporal and diel variations of fish assemblages at two sandy beaches in the Sepetiba bay, Rio de Janeiro, Brazil. Estuarine, Coastal and Shelf Science 57:817-828.; Oliveira-Neto et al., 2004Oliveira-Neto, J. F.; Godefroid, R. S.; Queiroz, G. M. L. N. & Schwarz, Jr. R. 2004. Variação diurna na captura de peixes em uma planície de maré da baía de Paranaguá, PR. Acta Biológica Leopoldensia 26(1):125-138.). Nocturnal habits of P. valenciennis could be attributed to its non-visual feeding mode (Gelós et al., 2010Gelós, M.; Teixeira-De-Mello, F.; Goyenola, G.; Iglesias, C.; Fosalba, C.; García-Rodríguez, F. J.; Pacheco, P.; García, S. & Meerhoff, M. 2010. Seasonal and diel changes in fish activity and potential cascading effects in subtropical shallow lakes with different water transparency. Hydrobiología 646:173-185.), and like other Siluriformes, it could present a nocturnal behavior (Fernández et al., 2007Fernández, D. R.; Agostinho, A. A.; Bini, L. M. & Pelicice, F. M. 2007. Diel variation in the ascent of fishes up an experimental fish ladder at Itaipu reservoir: fish size, reproductive stage and taxonomic group influences. Neotropical Ichthyology 5(2):215-222.). Salinity values were not registered during the night, however due to the freshwater ecology of the species, these could have been lower during the nocturnal period. Regarding the diel variability observed for B. aurea, results were consistent with those found by Barreiros et al. (2005Barreiros, J. P.; Figna, V.; Mauricio, V. F.; Silva, H. & Santos, R. S. 2005. Diel seasonality of a shallow water fish assemblage in a sandy beach at Canto Grande, Santa Catarina, Brazil. Journal of Coastal Research SI (42):343-347.) in southern Brazil, who observed higher densities of a closely related species, Brevoortia pectinata (Jenyns, 1842), during nighttime. Also, the species O. argentinensis presented daily differences in the Pando estuary, which may be attributed to its preference towards higher salinity values (Tombari et al., 2005Tombari, A. D.; Volpedo, A. V. & Echeverría, D. D. 2005. Desarrollo de la sagitta en juveniles y adultos de Odontesthes argentinensis (Valenciennes, 1835) y O. bonariensis (Valenciennes, 1835) de la provincia de Buenos Aires, Argentina (Teleostei: Atheriniformes). Revista Chilena de Historia Natural 78(4):623-633.). Gurdek et al. (2011Gurdek, R.; Muñoz, N.; Puppi, V.; Bianchinotti, V. & Acuña, A. 2011. Variación nictimeral de la ictiofauna de la región estuarial del arroyo Solís Grande, Uruguay. Boletín de la Sociedad Zoológica del Uruguay 20:11-21.) showed that Odontesthes sp. decreased in number towards the evening-night time in the Solís Grande sub-estuary, considering the photoperiod as the main influencing factor.

Turbidity might have affected the fish assemblage daily patterns. Diel differences in the fish composition were less evident during winter and autumn (with the lowest salinity values), compared to summer and spring. A strong inverse relationship between turbidity and salinity values has been suggested in estuaries (Cyrus & Blaber, 1992Cyrus, D. P. & Blaber, S. J. M. 1992. Turbidity and salinity in a tropical northern Australian estuary and their influence on fish distribution. Estuarine, Coastal and Shelf Science 35(6):545-563.). The same kind of relationship was observed in the Solís Grande sub-estuary (Rodrigo Gurdek, pers. observ.). In this sense, predation rates were reported to be highest in clear versus turbid waters because of visual cues, suggesting that of predation risk will be reduced in turbid aquatic ecosystems (Utne-Palm, 2002Utne-Palm, A. C. 2002. Visual feeding of fish in a turbid environment: physical and behavioural aspects. Marine and Freshwater Behaviour and Physiology 35(1-2):111-128.; De Robertis et al., 2003De Robertis, A.; Ryer, C. H.; Veloza, A. & Brodeur, R. D. 2003. Differential effects of turbidity on prey consumption of piscivorous and planktivorous fish. Canadian Journal of Fisheries and Aquatic Sciences 60:1517-1526.).

This work appears to be one of the few attempts to describe temporal patterns of estuarine use and diel variability of fish communities in a sub-estuarine environment. Presented findings included temporal changes in the fish community regarding seasonal and diel scales. Evidence of an extensive use of the system by juveniles was provided, mainly for M. furnieri, suggesting the nursery use of fish estuarine populations. Results in the Pando sub-estuary were in accordance with those found in estuaries. Future studies in sub-estuaries should take into account the diel variability according to different size classes of fish within littoral zones, as well as include a more intense seasonal and diel sampling regime. Sampling in different weather conditions rather than El Niño is also recommended. Findings will help to better understand the species and community dynamics as well as the ecological use of species in the sub-estuaries.

Acknowledgements

We would like to thank the people from IctioPando Project, who participated in field data collection and laboratory procedures: Federico Viana, Ruben Canavese, Cecilia Passadore, Agustín Carnikián, Julio Richly, Bibiana Musso, Matías Zarucki, Fabián Vásquez, Natalie Borba and Héctor Ferrando.

REFERENCES

  • Acha, E. M.; Mianzan, H.; Guerrero, R.; Carreto, J.; Giberto, D.; Montoya, N. & Carignan, M. 2008. An overview of physical and ecological processes in the Río de la Plata estuary. Continental Shelf Research 28:1579-1588.
  • Acuña, A. P.; Passadore, C. & Gimenez, L. 2010. Fish assemblage in a temperate estuary on the Uruguay coast: seasonal variation and environmental influence. Brazilian Journal of Oceanography 58(4):299-314.
  • Acuña, A. P.; Gurdek, R.; Muñoz, N.; Gutierrez, J. M.; Spósito, M.; Correa, P. & Caride, A. Seasonal composition, abundance and biomass of the subestuarine fish assemblage in Solís Chico (Río de la Plata estuary, Uruguay). Brazilian Journal of Biology. In press. http://dx.doi.org/10.1590/1519-6984.02216
    » https://doi.org/10.1590/1519-6984.02216
  • Akin, S.; Buhan, E.; Winemiller, K. O. & Yilmaz, H. 2005. Fish assemblage structure of Koycegiz lagoon-estuary, Turkey: Spatial and temporal distribution patterns in relation to environmental variation. Estuarine, Coastal and Shelf Science 64:671-684.
  • Albaret, J. J.; Simier, M.; Darboe, F. S.; Ecoutin, J. M.; Raffry, J. & de Morais, L. T. 2004. Fish diversity and distribution in the Gambia estuary, West Africa, in relation to environmental variables. Aquatic Living Resources 17:35-46.
  • Arceo-Carranza, D. & Vega-Cendejas, M. E. 2009. Spatial and temporal characterization of fish assemblages in a tropical coastal system influenced by freshwater inputs: northwestern Yucatan peninsula. Revista de Biología Tropical (International Journal of Tropical Biology and Conservation) 57(1-2):89-103.
  • Barletta, M.; Amaral, C. S.; Correa, M. F. M.; Guebert, F.; Dantas, D. V.; Lorenzi, L. & Saint-Paul, U. 2008. Factors affecting seasonal variations in demersal fish assemblages at an ecocline in a tropical-subtropical estuary. Journal of Fish Biology 73:1314-1336.
  • Barreiros, J. P.; Figna, V.; Mauricio, V. F.; Silva, H. & Santos, R. S. 2005. Diel seasonality of a shallow water fish assemblage in a sandy beach at Canto Grande, Santa Catarina, Brazil. Journal of Coastal Research SI (42):343-347.
  • Becker, A.; Cowley, P. D.; Whitfield, A. K.; Jarnegren, J. & Naesje, T. F. 2011. Diel fish movements in the littoral zone of a temporarily closed South African estuary. Journal of Experimental Marine Biology and Ecology 406:63-70.
  • Bidegain, M.; Caffera, F. R. M.; Blixen, F.; Pshennikov, V. J.; Lagomarsino, J.; Forbes, E. A. & Nagy, G. J. 2005. Tendencias climáticas, hidrológicas y oceanográficas en el Río de la Plata y costa uruguaya. In: Barros, V.; Menéndez, A. & Nagy, G. eds. El cambio climático en el Río de la Plata. Buenos Aires, CIM, CONICET, p. 137-143.
  • Bruno, D. O.; Barbini, S. A.; Astarloa, J. M. D. & Martos, P. 2013. Fish abundance and distribution patterns related to environmental factors in a choked temperate coastal lagoon (Argentina). Brazilian Journal of Oceanography 61:43-53.
  • Cardoso, I.; Franca, S.; Pais, M. P.; Henriques, S.; Fonseca, L. C. & Cabral, H. N. 2011. Fish assemblages of small estuaries of the Portuguese coast: A functional approach. Estuarine, Coastal and Shelf Science 93:40-46.
  • Castillo-Rivera, M.; Zárate-Hernández, R.; Ortiz-Burgos, S. & Zavala-Hurtado, J. 2010. Diel and seasonal variability in the fish community structure of a mud-bottom estuarine habitat in the Gulf of Mexico. Marine Ecology 31(4):633-642.
  • Cayssials, R.; Hernández, J.; Cantón, V.; Fernández, V.; Laborde, J. L. & Collazo, D. 2000. Caracterización del medio físico. In: Laborde, J. L.; Perdomo, A. & Gómez-Erache, M. eds. Diagnóstico ambiental y socio-demográfico de la zona costera uruguaya del Río de la Plata. Montevideo, Ecoplata, p. 14-73.
  • Clarke, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18:117-143.
  • Clark, K. L.; Ruiz, G. M. & Hines, A. H. 2003. Diel variation in predator abundance, predation risk and prey distribution in shallow-water estuarine habitats. Journal of Experimental Marine Biology and Ecology 287:37-55.
  • Cyrus, D. P. & Blaber, S. J. M. 1992. Turbidity and salinity in a tropical northern Australian estuary and their influence on fish distribution. Estuarine, Coastal and Shelf Science 35(6):545-563.
  • Day, J. W.; Crump, Jr. B. C.; Kemp, W. M. & Yáñez-Arancibia, A. 2013. Estuarine Ecology. Hoboken, Wiley-Blackwell, John Wiley & Sons. 500p.
  • De Robertis, A.; Ryer, C. H.; Veloza, A. & Brodeur, R. D. 2003. Differential effects of turbidity on prey consumption of piscivorous and planktivorous fish. Canadian Journal of Fisheries and Aquatic Sciences 60:1517-1526.
  • Dyer, B. S. H. 2006. Systematic revision of the South American silversides (Teleostei, Atheriniformes). Biocell 30(1):69-88.
  • Fernández, D. R.; Agostinho, A. A.; Bini, L. M. & Pelicice, F. M. 2007. Diel variation in the ascent of fishes up an experimental fish ladder at Itaipu reservoir: fish size, reproductive stage and taxonomic group influences. Neotropical Ichthyology 5(2):215-222.
  • Figueiredo, J. L. & Menezes, N. A. 1978. Manual de peixes marinhos do sudeste do Brasil. II. Teleostei (1). São Paulo, Museu de Zoologia da Universidade de São Paulo. 110p.
  • Figueiredo, J. L. & Menezes, N. A. 1980. Manual de peixes marinhos do sudeste do Brasil. III. Teleostei (2). São Paulo, Museu de Zoologia da Universidade de São Paulo . 98p.
  • Figueiredo, J. L. & Menezes, N. A. 2000. Manual de peixes marinhos do sudeste do Brasil. VI. Teleostei (5). São Paulo, Museu de Zoología da Universidade de São Paulo. 116p.
  • Franca, S.; Costa, M. J. & Cabral, H. N. 2011. Inter- and intra-estuarine fish assemblage variability patterns along the Portuguese coast. Estuarine, Coastal and Shelf Science 91:262-271.
  • Gaelzer, L. R. & Zalmon, I. R. 2008. Diel Variation of fish community in sandy beaches of southeastern Brazil. Brazilian Journal of Oceanography 56:23-39.
  • García, M. L.; Jaureguizar, A. J. & Protogino, L. C. 2010. From fresh water to the slope: fish community ecology in the Río de la Plata and the sea beyond. Latin American Journal of Aquatic Research 38(1):81-94.
  • Gelós, M.; Teixeira-De-Mello, F.; Goyenola, G.; Iglesias, C.; Fosalba, C.; García-Rodríguez, F. J.; Pacheco, P.; García, S. & Meerhoff, M. 2010. Seasonal and diel changes in fish activity and potential cascading effects in subtropical shallow lakes with different water transparency. Hydrobiología 646:173-185.
  • Greenwood, M. F. D.; Matheson, Jr. R. E.; McMichael, Jr. R. H. & MacDonald, T. C. 2007. Community structure of shoreline nekton in the portion of the Alafia river, Florida: Differences along a salinity gradient and inflow-related changes. Estuarine, Coastal and Shelf Science 74:223-238.
  • Gurdek, R.; Muñoz, N.; Puppi, V.; Bianchinotti, V. & Acuña, A. 2011. Variación nictimeral de la ictiofauna de la región estuarial del arroyo Solís Grande, Uruguay. Boletín de la Sociedad Zoológica del Uruguay 20:11-21.
  • Gurdek, R.; De La Rosa, A.; Corrales, D.; Canavese, R.; Gutierre, J. M.; Stebniki, S.; Muñoz, N.; Severi, V. & Acuña-Plavan, A. 2016. Estuarine use and composition of fish species in the Solís Grande sub-estuary, Uruguay. Pan-American Journal of Aquatic Sciences 11(1):82-86.
  • Hagan, S. M. & Able, K. W. 2003. Seasonal changes of the pelagic fish assemblage in a temperate estuary. Estuarine, Coastal and Shelf Science 56:15-29.
  • Hoeksema, S. D. & Potter, I. C. 2006. Diel, seasonal, regional and annual variations in the characteristics of the ichthyofauna of the upper reaches of a large Australian microtidal estuary. Estuarine, Coastal and Shelf Science 67:503-520.
  • Idelberger, C. F. & Greenwood, M. F. D. 2005. Seasonal variation in fish assemblages within the estuarine portions of the Myakka and Peace rivers, southwest Florida. Gulf of Mexico Science 2:224-240.
  • James, N. C.; Whitfield, A. K. & Cowley, P. D. 2008. Long-term stability of the fish assemblages in a warm-temperate South African estuary. Estuarine, Coastal and Shelf Science 76:723-738.
  • Jaureguizar, A. J.; Menni, R.; Guerrero, R. & Lasta, C. 2004. Environmental factors structuring fish communities of the Río de la Plata estuary. Fisheries Research 66:195-211.
  • Loebmann, D.; Vieira, J. P.; Bemvenuti, M. A.; Astarloa, J. M. D.; Cousseau, M. B. & Figueroa, D. 2008. Composição e abundância da ictiofauna de duas lagunas costeiras da América do Sul Austral: lagoa do Peixe (31°S; 51°W), Brasil e laguna Mar Chiquita (37°S; 57°W), Argentina. Neotropical Biology and Conservation 3:28-33.
  • Macchi, G. J.; Acha, M. E. & Lasta, C. A. 1996. Desove y fecundidad de la corvina rubia Micropogonias furnieri Desmarest, 1823 del estuario del Río de la Plata, Argentina. Boletín Instituto Español de Oceanografía 12(2):99-113.
  • McLusky, D. S. & Elliott, M. 2004. The estuarine ecosystem: ecology, threats and management. New York, Oxford University Press. 214p.
  • Menezes, N. A. & Figueiredo, J. L. 1980. Manual de peixes marinhos do sudeste do Brasil. IV. Teleostei (3). São Paulo, Museu de Zoologia da Universidade de São Paulo . 96p.
  • Menezes, N. A. & Figueiredo, J. L. 1985. Manual de peixes marinhos do sudeste do Brasil. V. Teleostei (4). São Paulo, Museu de Zoologia da Universidade de São Paulo . 96p.
  • Menni, R. C.; Ringuelet, R. A. & Aramburu, R. H. 1984. Peces marinos de la Argentina y Uruguay. Buenos Aires, Editorial Hemisferio Sur. 359p.
  • Methven, D. A.; Haedrich, R. L. & Rose, G. A. 2001. The fish assemblage of a Newfoundland estuary: diel, monthly and annual variation. Estuarine, Coastal and Shelf Science 52:669-687.
  • Mtop-Pnud, 1979. Proyecto sobre conservación y mejora de playas (URU. 73007). Montevideo, Ministerio de Transporte y Obras Públicas, UNESCO. 593p.
  • Oliveira-Neto, J. F.; Godefroid, R. S.; Queiroz, G. M. L. N. & Schwarz, Jr. R. 2004. Variação diurna na captura de peixes em uma planície de maré da baía de Paranaguá, PR. Acta Biológica Leopoldensia 26(1):125-138.
  • Oliveira-Neto, J. F.; Spach, H. L.; Schwarz-Junior, R. & Pichler, H. A. 2008. Diel variation in fish assemblages in tidal creeks in southern Brazil. Brazilian Journal of Biology 68(1):37-43.
  • Pasquaud, S.; Vasconcelos, R. P.; Franca, S.; Henriques, S.; Costa, M. J. & Cabral, H. N. 2015. Worldwide patterns of fish biodiversity in estuaries: effect of global vs. local factors. Estuarine, Coastal and Shelf Science 154:122-128.
  • Pessanha, A. L. M. & Araújo, F. G. 2003. Spatial, temporal and diel variations of fish assemblages at two sandy beaches in the Sepetiba bay, Rio de Janeiro, Brazil. Estuarine, Coastal and Shelf Science 57:817-828.
  • Potter, I. C.; Beckley, L. E.; Whitfield, A. K. & Lenanton, R. C. J. 1990. Comparisons between the roles played by estuaries in the life cycles of fishes in temperate Western Australia and Southern Africa. Environmental Biology of Fishes 28:143-178.
  • Potter, I. C. & Hyndes, G. A. 1999. Characteristics of the ichthyofaunas of southwestern Australian estuaries, including comparisions with holarctic estuaries and estuaries elsewhere in temperate Australia: A review. Australian Journal of Ecology 24:395-421.
  • Retta, S.; Martinez, G. & Errea, A. 2006. Área de cría de peces en la costa uruguaya. In: Menafra, R.; Rodriguez-Gallego, L.; Scarabino, F. & Conde, D. eds. Bases para la conservación y el manejo de la costa uruguaya. Montevideo, Vida Silvestre, p. 221-218.
  • Ribeiro, J.; Bentes, L.; Coelho, R.; Gonçalves, J. M. S.; Lino, P. G.; Monteiro, P. & Erzini, K. 2006. Seasonal, tidal and diurnal changes in fish assemblages in the Ria Formosa lagoon (Portugal). Estuarine, Coastal and Shelf Science 67:461-474.
  • Ringuelet, R. A.; Aramburu, R. H. & De Aramburu, A. A. 1967. Los peces argentinos de agua dulce. La Plata, Comisión de Investigación Científica. 602p.
  • Selleslagh, J. & Amara, R. 2008. Environmental factors structuring fish composition and assemblages in a small macrotidal estuary (eastern English Channel). Estuarine, Coastal and Shelf Science 79:507-517.
  • Shapiro, S. S. & Wilk, M. B. 1965. An analysis of variance test for normality (Complete samples). Biometrika 52:591-611.
  • Simier, M.; Laurent, C.; Ecoutin, J. & Albaret, J. 2006. The Gambia River estuary: a reference point for estuarine fish assemblages studies in West Africa. Estuarine, Coastal and Shelf Science 69:615-628.
  • Sokal, R. R. & Rohlf, J. F. 1969. Biometria. New York, Freeman W.H. and Company. 832p.
  • Thiel, R.; Sepúlveda, A.; Kafemann, R. & Nellen, W. 1995. Environmental factors as forces structuring the fish community of the Elbe Estuary. Journal of Fish Biology 46:47-69.
  • Tombari, A. D.; Volpedo, A. V. & Echeverría, D. D. 2005. Desarrollo de la sagitta en juveniles y adultos de Odontesthes argentinensis (Valenciennes, 1835) y O. bonariensis (Valenciennes, 1835) de la provincia de Buenos Aires, Argentina (Teleostei: Atheriniformes). Revista Chilena de Historia Natural 78(4):623-633.
  • Utne-Palm, A. C. 2002. Visual feeding of fish in a turbid environment: physical and behavioural aspects. Marine and Freshwater Behaviour and Physiology 35(1-2):111-128.
  • Whitfield, A. K. 1999. Ichthyofaunal assemblages in estuaries: A South African case study. Reviews in Fish Biology and Fisheries 9:151-186.
  • Zárate-Hernández, R.; Castillo-Rivera, M.; Sanvicente-Añorve, L. & Ortiz-Burgos, S. 2012. Spatial, diel, and seasonal changes in the fish community structure of a Mexican tropical estuary. Ciencias Marinas 38(4):665-676.

Publication Dates

  • Publication in this collection
    2017

History

  • Received
    02 Mar 2016
  • Accepted
    30 Sept 2016
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