INTRODUCTIONTop

The ichthyofauna can be described and classified through the functional attributes of organisms, mainly based on the trophic level, reproductive strategy or use of the environment (Elliott et al. 2007Elliott M., Whitfield A.K., Potter I.C., et al. 2007. The guild approach to categorizing estuarine fish assemblages: A global review. Fish Fish. 8: 241-268.). The functional attributes divide the species into guilds, defined as groups of species that exploit the same class of environmental resources in a similar way (Root 1967Root R.B. 1967. The niche exploitation pattern of the blue-gray gnatcatcher. Ecol. Monographs 37: 317-350.). The guild approach allows a better understanding of the ecology and role of the biota in the ecosystem (Elliott et al. 2007Elliott M., Whitfield A.K., Potter I.C., et al. 2007. The guild approach to categorizing estuarine fish assemblages: A global review. Fish Fish. 8: 241-268.). It may help identify overexploited resources through changes in the composition of the food web (Garrison and Link 2000Garrison L.P., Link J. 2000. Fishing effects on spatial distribution and trophic guild structure of the fish community in the Georges Bank region. ICES J. Mar. Sci. 57: 723-730.) and of the energy flows in the system (Harrison and Whitfield 2008Harrison T.D., Whitfield A.K. 2008. Geographical and typological changes in fish guilds of South African estuaries. J. Fish Biol. 73: 2542-2570.). The guild approach also helps to understand the effects of climate changes on the structure and composition of fish fauna (Feyrer et al. 2015Feyrer F., Cloern J.E., Brown L.R., et al. 2015. Estuarine fish communities respond to climate variability over both river and ocean basins. Glob. Chang. Biol. 21: 3608-3619.).

Trophic and estuarine use guilds have been widely applied to understand the structure and functioning of aquatic ecosystems, the movement pattern between environments and their use as feeding, breeding or development grounds (Elliott et al. 2007Elliott M., Whitfield A.K., Potter I.C., et al. 2007. The guild approach to categorizing estuarine fish assemblages: A global review. Fish Fish. 8: 241-268.). Estuarine use guilds reflect migratory patterns and physiological adaptations of species that explore the area throughout their life cycle or part of it (Elliott et al. 2007Elliott M., Whitfield A.K., Potter I.C., et al. 2007. The guild approach to categorizing estuarine fish assemblages: A global review. Fish Fish. 8: 241-268.). Trophic guilds are useful in the comprehension of the feeding habits of a species (Elliott et al. 2007Elliott M., Whitfield A.K., Potter I.C., et al. 2007. The guild approach to categorizing estuarine fish assemblages: A global review. Fish Fish. 8: 241-268.). Its ecological relationships and the energy flows (Paiva et al. 2008Paiva A.C.G., Chaves P.D.T.D.C., Araújo M.E. 2008. Estrutura e organização trófica da ictiofauna de águas rasas em um estuário tropical. Rev. Bras. Zool. 25: 647-661.) may reflect the possible strategies for avoiding competition or for optimizing the consumption of available resources (Angel and Ojeda 2001Angel A., Ojeda F.P. 2001. Structure and trophic organization of subtidal fish assemblages on the northern Chilean coast: the effect of habitat complexity. Mar. Ecol. Prog. Ser. 217: 81-91.).

Estuaries are important transitional environments for the movement of the ichthyofauna between the continental basins and the ocean (Ray 2005Ray G.C. 2005. Connectivities of estuarine fishes to the coastal realm. Estuar. Coast. Shelf Sci. 64: 18-32.). As an ecotone, estuaries link marine and freshwater ecosystems (Gray and Elliott 2009Gray J.S., Elliott M. 2009. Ecology of Marine Sediments: From Science to Management. Oxford Univ. Press, NY, 256 pp.), and persistent environmental fluctuations place considerable physiological demands on the species inhabiting the area (Elliott and Quintino 2007Elliott M., Quintino V. 2007. The estuarine quality paradox, environmental homeostasis and the difficulty of detecting anthropogenic stress in naturally stressed areas. Mar. Pollut. Bull. 54: 640-645.). Many species are dependent on estuarine environments; several marine species are considered visitors and explore estuarine habitats during their ontogenetic development, evidencing the relationship with coastal environments (Able 2005Able K.W., Fahay M.P., Witting D.A., et al. 2005. Fish settlement in the ocean vs. estuary: Comparison of pelagic larval and settled juvenile composition and abundance. Estuar. Coast. Shelf Sci. 66: 280-290.). Therefore, defining the relationships between species and their functional roles within communities is critical for understanding the dynamics of the ecosystem and fundamental for the implementation of ecosystem-based fisheries management (Buchheister and Latour 2015Buchheister A., Latour R.J. 2015. Diets and trophic-guild structure of a diverse fish assemblage in Chesapeake Bay, U.S.A. J. Fish Biol. 86: 967-992.).

The Brazilian coast hosts large estuarine complexes along the 187 km of the coast of Pernambuco, and several areas are considered of great environmental importance (CPRH 2010CPRH. Agência Estadual de Meio Ambiente. 2010. Diagnóstico Sócio ambiental da Área de Proteção Ambiental de Santa Cruz. Companhia Pernambucana de Meio Ambiente, Recife, 388 pp.). The variety of habitats, along with the complexity of interactions within the fish community and the migratory nature of many species, hampers the assessment of the overall condition of the area (Vasconcelos Filho et al. 2003Vasconcelos Filho A.L., Neumann-Leitão S., Eskinazi-Leça E., et al. 2003. Trophic interactions between fish and other compartment communities in a tropical estuary in Brazil as indicator of environmental quality. Adv. Ecol. Sci. 18: 173-183.).

Using the ecological guilds approach, this study describes the composition and structure of the fish fauna along a tropical estuarine complex in order to identify and explain the main patterns of seasonal and spatial variations in assemblage composition. The study also discusses the importance of the use of the ecological guilds approach to assess the effects of multiple anthropogenic pressures on the structure and functioning of fish communities in tropical estuaries.

MATERIALS AND METHODSTop

Study area

The Itapissuma/Itamaracá Complex (IIC), located in Pernambuco, northeastern Brazil, within the Santa Cruz Environmental Preservation Area (APA Santa Cruz), is considered highly productive (Macêdo et al. 2000Macêdo S.J., Flores Montes M.J., Lins I.C. 2000. Características abióticas da área. In: Barros H.M., Eskinazi-Leça E., Macêdo S.J., et al. (eds), Gerenciamento participativo de estuários e manguezais. UFPE, Recife, pp. 7-25.), hosting the largest fishery port in the state. Fishery is a very important socio-economical activity in the IIC, generating income and proteins for the local communities (CPRH 2010CPRH. Agência Estadual de Meio Ambiente. 2010. Diagnóstico Sócio ambiental da Área de Proteção Ambiental de Santa Cruz. Companhia Pernambucana de Meio Ambiente, Recife, 388 pp.). Conversely, this ecosystem is exposed to multiple pressures from industrial pollution, domestic sewage discharge, urban expansion, land reclamation and fisheries (Medeiros et al. 2001Medeiros C., Kjerfve B., Araújo Filho M., et al. 2001. The Itamaracá Estuarine Ecosystem, Brazil. In: Seelinger U., Kjerfve B. (eds), Ecological Studies: Coastal Marine Ecosystems of Latin America. Springer-Verlag, New York, pp. 71-81.). In addition, it has a large variety of connecting habitats favouring the development of the ichtyofauna (Vasconcelos Filho et al. 2009Vasconcelos Filho A.L., Neumann-Leitão S., Eskinazi-Leça E., et al. 2009. Hábitos alimentares de consumidores primários da ictiofauna do sistema estuarino de Itamaracá (Pernambuco - Brasil). Rev. Bras. Eng. Pesca 4: 21-31). The IIC is composed of the estuarine area, the Santa Cruz Channel and the adjacent sea, locally named the “Inner Sea” (Fig. 1). The Santa Cruz channel has a length of 22 km, a width ranging from 0.6 to 1.5 km and a depth ranging from 2 to 5 m in the central part of the channel, reaching 10 m at the northern and southern bars that connect the channel to the sea (Vasconcelos Filho and Oliveira 1999Vasconcelos Filho A.L., Oliveira A.M.E. 1999. Composição e ecologia da ictiofauna do Canal de Santa Cruz (Itamaracá-PE, Brasil). Trab. Ocean. UFPE 27: 101-113). The channel bottom consists of quartz sand banks and dark, reductive and dense mud patches. The muddy banks are dominated by Rhyzophora mangle, Laguncularia racemosa, Avicennia sp. and Conocarpus erectus, and by meadows of the marine phanerogam, Halodule wrightii. Surface water temperature varies between 25°C and 31°C and salinity between 18 and 34. The Inner Sea, corresponding to the coastal area hereafter, with a depth of 2 to 5 m, is characterized by a reef barrier parallel to the coast, located 4 km from the beach (Kempf 1970Kempf M. 1970. Nota preliminar sobre os fundos costeiros da região de Itamaracá (Norte do Estado de Pernambuco, Brasil). Trab. Oceanog. Univ. Fed. Pernambuco 11: 95-111.), which functions as a barrier between nearshore and shelf waters. The substrate is formed by terrigenous sediments from the mouth of the Jaguaribe River and the Santa Cruz Channel, and carbonates from the reef barrier (Almeida and Manso 2011Almeida T.L.M., Manso V.A.V. 2011. Sedimentologia da plataforma interna adjacente a Ilha de Itamaracá - Pe. Est. Geol. 21: 135-152.), partially covered by large banks of phanerogams (Kempf 1970Kempf M. 1970. Nota preliminar sobre os fundos costeiros da região de Itamaracá (Norte do Estado de Pernambuco, Brasil). Trab. Oceanog. Univ. Fed. Pernambuco 11: 95-111.). The carbonaceous material is the result of the decomposition of rocks and quartz, sand, mollusc shells, foraminifera and calcareous algal fragments. In the Inner Sea, water temperature varies between 27°C and 30.8°C and the average annual salinity is 34.

Data collection

Fish specimens were collected during the dry season (January, February, March, November) and the rainy season (May, July, August) in 2013 and 2014 in the Santa Cruz Channel and the Inner Sea. In order to minimize biases due to gear selectivity, different fishing gears were combined for accessing and sampling different habitats and maximizing the collection of fish individuals (Table S1, Supplementary material). In the estuary, three 25-minute sets with a seine net and one 6-hour set with a block net were carried out quarterly. The seine net was 67.5 m long and had a mesh size of 10 mm. The block net was 348 m long and had a mesh size of 60, 70 and 80 mm. On the coast, samples were obtained quarterly with a gillnet (3 sets of two hours each) and with a fixed tidal trap (6 fishing days). The gill net had mesh sizes of 50, 70 and 80 mm, and was 690 m long, and the fixed tidal trap had a diameter of 27 m and a mesh size of 70 mm.

In the field, the fish fauna was conserved in thermal boxes with ice, and samples were frozen in the laboratory to be identified. Taxonomic classification followed Nelson et al. (2016)Nelson J.S., Grande T.C., Wilson M.V.H. 2016. Fishes of the world. Wiley & Sons, New Jersey, 299 pp..

Data analysis

Firstly, we computed a species accumulation curve with the non-parametric Bootstrap method (Smith and van Belle 1984Smith E.P., van Belle G. 1984. Nonparametric Estimation of Species Richness. Biometrics 40: 119-129.) to assess whether the fish community was exhaustively sampled. This method assumes that all species occur randomly without taking into account species abundance, i.e. the method does not distinguish rare and abundant species (Smith and van Belle 1984Smith E.P., van Belle G. 1984. Nonparametric Estimation of Species Richness. Biometrics 40: 119-129.). The index and standard deviations of the estimates were obtained through the analytical equation of Colwell et al. (2004)Colwell R.K., Mao C.X., Chang J. 2004. Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85: 2717-2727. using the EstimateS software v. 9 9.1.0 (Colwell 2013Colwell R.K. 2013. EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. User’s Guide and application at http://purl.oclc.org/estimates).

The composition of the fish fauna was reported in terms of absolute species richness (S) and, for each species, frequency of occurrence (%FO) and relative abundance in number (%N) and biomass (%B). Species were considered to be abundant according to the Garcia and Vieira (2001)Garcia A.M., Vieira J.P. 2001. O aumento da diversidade de peixes no estuário da Lagoa dos Patos durante o episódio El Niño 1997-1998. Atlântica 23: 133-152. classification when %N was greater than 100/S, where S is the number of species recorded in the area. A species was defined as frequent when its %FO value for a given area was greater than 50%. The combination of these parameters allowed the species to be classified into four categories: abundant and frequent (%N>100/S and %FO≥50%); abundant but infrequent (%N>100/S and %FO<50%); less abundant but frequent (%N<100/S and %FO≥50%) and less abundant and infrequent (%N<100/S and %FO<50%).

Each species was assigned to an estuarine use functional group: marine stragglers, marine migrants and estuarine species, according to the classification proposed by Elliott et al. (2007)Elliott M., Whitfield A.K., Potter I.C., et al. 2007. The guild approach to categorizing estuarine fish assemblages: A global review. Fish Fish. 8: 241-268.. This classification is based on the type, frequency and period of use of the estuarine environment, and the abundance of the species in the estuary. In addition, each species was assigned to a trophic functional group based on local information about feeding preferences and strategies, according to the categories proposed by Elliott et al. (2007)Elliott M., Whitfield A.K., Potter I.C., et al. 2007. The guild approach to categorizing estuarine fish assemblages: A global review. Fish Fish. 8: 241-268.. The trophic functional groups were zooplanktivores, detritivores, piscivores, zoobenthivores, herbivores and omnivores. Information on trophic guilds were obtained in studies carried out in the IIC, in the scientific literature or, when not available, based on the WoRMS Editorial Board (2019)WoRMS Editorial Board. 2019. World Register of Marine Species. Accesed on 10/02/2019, at http://www.marinespecies.org/ and FishBase project (Froese and Pauly 2007Froese R., Pauly D. 2007. FishBase. Version 06/2018. http://www.fishbase.org) (Table S2, Supplementary material). For each environment (estuary and coast) and season (dry and rainy), the estuarine use guild and the trophic guild were reported in terms of richness (%S), abundance (%N) and biomass (%B).

We computed multivariate analyses to investigate the spatial and temporal variations in the structure of the fish community, considering the absolute richness of estuarine use guild and the richness of trophic guild by environment and by season. To analyse the guild composition, a principal coordinate analysis (PCO) based on Bray-Curtis distances was applied. The differences of the contribution of guilds between environments and seasons was tested by permutational multivariate analysis (PERMANOVA) (Anderson 2001Anderson M.J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26: 32-46.) performed with a Bray-Curtis distance matrix built on square-root-transformed data. Multivariate analyses were performed with the R software (R Core Team 2018R Core Team. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.).

RESULTSTop

Fish assemblage

A total of 140 species (135 Actinopterygii and 5 Elasmobranchii) of 34 families were recorded in the IIC (Table 1). For both coastal and estuarine areas, the species accumulation curve did not stabilize towards asymptotic values (Fig. S1, Supplementary material). However, a large portion of the estimated richness was effectively sampled: 88 species (88% of the estimated richness) were observed in the estuary and 75 species (85% of the estimated richness) on the coast. A total of 25 species (18%) were common to both the estuary and the coast, 65 species (47%) were exclusive to the estuary and 50 species (35%) occurred only on the coast (Table 1).

In the estuary, Engraulidae (9 species), Gerreidae (9 species) and Gobiidae (8 species) were dominant in richness (S). The Gobiidae family had the highest abundance (%N) in the dry (7694 individuals, 62%) and rainy (3776 individuals, 58%) seasons. In terms of biomass, Mugilidae were dominant during the dry season (114.34 kg, 51.74%) and Gobiidae during the rainy season (22.20 kg, 28%). The gobiid Gobionelus stomatus Starks, 1913 showed the highest abundance in both seasons (dry season 6582 individuals, 53%; rainy season 3532 individuals, 54%), while for biomass, Mugil curema Valenciennes, 1836 (114.39 kg, 52%) and Cetengraulis edentulus (Spix and Agassiz, 1829) (18 kg, 22.42%) were dominant during the dry and the rainy seasons, respectively (Table 1).

On the coast, Carangidae were dominant in richness (14 species); in abundance, with 288 individuals (49%) and 166 individuals (50%) during the dry and rainy seasons, respectively; and in biomass, with 115 kg (57%) and 203 kg (74%) in the dry and rainy seasons, respectively. In terms of species, Selene brownii (Cuvier, 1816) was dominant with the highest abundance d,uring the dry season (138 individuals; 23%) and Selene vomer (Linnaeus, 1758) during the rainy season (45 individuals, 14%), while Trichiurus lepturus Linnaeus, 1758 (26 kg, 13%) and Caranx hippos (Linnaeus, 1766) (151.59 kg, 55%) dominated in terms of biomass during the dry and the rainy seasons, respectively (Table 1).

Less abundant and infrequent species were dominant in the estuary (85%) and on the coast (77%) (Table 1). Eucinostomus argenteus Baird and Girard, 1855, Eucinostomus gula (Quoy and Gaimard, 1824), Ctenogobius smaragdus (Valenciennes, 1837), Ctenogobius stigmaticus (Poey, 1860), Gobionellus oceanicus (Pallas, 1770), G. stomatus and Sphoeroides testudineus (Linnaeus, 1758) were considered abundant and frequent in the estuary, and S. vomer in the coastal area.

Estuarine use structure

Richness, abundance and biomass of the estuarine use guilds did not vary by season, but differences were observed between the estuary and the coast. In the estuary, marine stragglers and marine migrants dominated in richness during the dry season (33 species, 43%) and the rainy (23 species, 41%). Estuarine species showed the highest abundance in the dry season (8150 individuals, 66%) and the rainy season (4099 individuals, 64%), but in terms of biomass, marine migrants dominated throughout the year (Fig. 2). On the coast, marine stragglers were dominant in richness (38 species, 70%; 31 species, 65%), in abundance (458 individuals, 78%; 259 individuals, 79%) and in biomass (147 kg, 76%; 238 kg, 90%) in the dry and rainy seasons, respectively (Fig. 2).

The PCO analysis based on the estuarine use guilds revealed that the main effect along the first axis (82.07 %) was spatial as it discriminated the samples from the coast and the estuary. Estuarine samples were very similar between seasons, whereas coastal samples showed a more heterogeneous pattern (Fig. 3). The patterns were tested through PERMANOVA and confirmed the location (estuary and coast) effect (p<0.05). No seasonal effect was observed (Table 2, p=0.01).

Trophic structure

Zoobenthivores were the richest trophic guild in the estuary: 38 species (41%) and 28 species (30%) in the dry and rainy seasons, respectively. The detritivores showed the highest abundance (15452 individuals, 62%; 10176 individuals, 53) and biomass (203 kg, 70; 82 kg, 47%) in the dry and rainy seasons, respectively (Fig. 4). On the coast, zoobenthivores also dominated in richness (30 species, 55.5%; 34 species, 60.1%) and abundance (372 individuals, 63.3%; 229 individuals, 50%), and piscivores had the greatest biomass (96 kg, 49%; 188 kg, 66.9%) in the dry and rainy seasons, respectively (Fig. 4).

The PCO based on trophic guilds discriminated samples from the estuary and from the coast along axis 1 (69.64%). In the estuary, differences were observed between the dry and rainy seasons (Fig. 5).

According to the PERMANOVA, the environments (estuary and coast) significantly influenced the abundance of the trophic guilds in the IIC (Table 3, p=0.004), confirming the groups formed by PCO (Fig. 5).

DISCUSSIONTop

Overall, species composition of the IIC was similar to that of the fish fauna typically found in other tropical estuaries (Paiva et al. 2008Paiva A.C.G., Chaves P.D.T.D.C., Araújo M.E. 2008. Estrutura e organização trófica da ictiofauna de águas rasas em um estuário tropical. Rev. Bras. Zool. 25: 647-661., Mourão et al. 2014Mourão K.R.M., Ferreira V., Lucena-Frédou F. 2014. Composition of functional ecological guilds of the fish fauna of the internal sector of the amazon estuary, pará, Brazil. An. Acad. Bras. Cienc. 86: 1783-1800.). The observed species richness was close to the estimated richness, indicating that sampling was satisfactory, thanks to the concomitant implementation of active and passive fishing gear. Sampling is known to affect catch composition, especially its diversity (Magurran and McGill 2011Magurran A.E., McGill B.J. 2011. Biological Diversity - Frontiers in Measurement and Assessment. Oxford Univ. Press, New York, 345 pp.), but the use of different gears provides the best estimate of structure (Kwak and Peterson 2007Kwak T.J., Peterson J.T. 2007. Community indices, parameters, and comparisons. In: Guy C.S., Brown M.L. (eds), Analysis and interpretation of freshwater fisheries data. American Fisheries Society, Maryland, pp. 677-763., Mourão et al. 2014Mourão K.R.M., Ferreira V., Lucena-Frédou F. 2014. Composition of functional ecological guilds of the fish fauna of the internal sector of the amazon estuary, pará, Brazil. An. Acad. Bras. Cienc. 86: 1783-1800.) and diversity of fish assemblages (Mérigot et al. 2016Mérigot B., Frédou F.L., Viana A.P., et al. 2016. Fish assemblages in tropical estuaries of northeastern Brazil: A multi-component diversity approach. Ocean Coast. Manag. 143: 175-183.). Different gears use different capture processes, mainly based on fish behaviour (Huse et al. 1999Huse I., Gundersen A.C., Nedreaas K.H. 1999. Relative selectivity of Greenland halibut (Reinhardtius hippoglossoides, Walbaum) by trawls, longlines and gillnets. Fish. Res. 44: 75-93.). In this study, the use of multiple gears was necessary, considering the differential characteristics of each environment sampled and the fact that fish species explore different habitats of a given environment differently. By exploring multiple gears in different habitats, we improved the estimation of biodiversity, thus providing as wide a variety of guilds as possible.

PCO analysis and PERMANOVA showed spatial differences in the estuarine use functional group between the estuarine and coastal areas, but temporal variations were not evidenced. Spatial segregation processes were observed in other tropical estuaries (Mourão et al. 2014Mourão K.R.M., Ferreira V., Lucena-Frédou F. 2014. Composition of functional ecological guilds of the fish fauna of the internal sector of the amazon estuary, pará, Brazil. An. Acad. Bras. Cienc. 86: 1783-1800., Loureiro et al. 2016Loureiro S.N., Reis-Filho J.A., Giarrizzo T. 2016. Evidence for habitat-driven segregation of an estuarine fish assemblage. J. Fish Biol. 55: 804-820.) and may be related to differences in the life cycle and in species tolerance to diverse environmental stresses. Temporal changes in the composition of estuarine fish communities were not observed in the IIC, as reported in other tropical estuaries (Castillo-Rivera et al. 2002Castillo-Rivera M., Zavala-Hurtado J.A., Zárate R. 2002. Exploration of spatial and temporal patterns of fish diversity and composition in a tropical estuarine system of Mexico. Rev. Fish Biol. Fish. 12: 167-177., Mendoza et al. 2009Mendoza E., Castillo-Rivera M., Zárate-Hernández R., et al. 2009. Seasonal variations in the diversity, abundance, and composition of species in an estuarine fish community in the Tropical Eastern Pacific, Mexico. Ichthyol. Res. 56: 330-339.).

In the estuary, migrant species predominated in richness and biomass, and estuarine species in abundance. The high richness and biomass of marine species in the estuary can be attributed to the permanent connection between the estuarine area and the Atlantic Ocean throughout the year (Medeiros and Kjerfve 1993Medeiros C., Kjerfve B. 1993. Hidrology of a tropical estuarine system: Itamaracá, Brazil. Estuar. Coast. Shelf Sci. 36: 495-515.), allowing an uninterrupted connectivity with the marine ecosystem (Vasconcelos et al. 2015Vasconcelos R.P., Henriques S., França S., et al. 2015. Global patterns and predictors of fish species richness in estuaries. J. Anim. Ecol. 84: 1331-1341.). Migratory species are of great importance in connected systems, such as estuaries and the adjacent marine area (Harrison and Whitfield 2008Harrison T.D., Whitfield A.K. 2008. Geographical and typological changes in fish guilds of South African estuaries. J. Fish Biol. 73: 2542-2570.). In addition, the IIC is considered a system with high biodiversity and primary and secondary productivity (Vasconcelos Filho et al. 2010Vasconcelos Filho A.L., Neumann-Leitão S., Eskinazi-Leça E., et al. 2010. Hábitos alimentares de peixes consumidores secundários do Canal de Santa Cruz, Pernambuco, Brasil. Trop. Oceanogr. 38: 121-128., Mérigot et al. 2016Mérigot B., Frédou F.L., Viana A.P., et al. 2016. Fish assemblages in tropical estuaries of northeastern Brazil: A multi-component diversity approach. Ocean Coast. Manag. 143: 175-183.). The positive effect of primary productivity on species richness allows larger populations to persist, thereby reducing extinction risk and supporting a higher diversity of niche specialists (Tittensor et al. 2010Tittensor D., Mora C., Jetz W., et al. 2010. Global patterns and predictors of marine biodiversity across taxa. Nature 466: 1098-1101.). According to Vasconcelos Filho and Oliveira (1999)Vasconcelos Filho A.L., Oliveira A.M.E. 1999. Composição e ecologia da ictiofauna do Canal de Santa Cruz (Itamaracá-PE, Brasil). Trab. Ocean. UFPE 27: 101-113, marine species of the IIC are mostly juveniles, some of which are of commercial value. The high abundance of estuarine species within the estuary of the IIC was mainly due to gobiids. Mérigot et al. (2016)Mérigot B., Frédou F.L., Viana A.P., et al. 2016. Fish assemblages in tropical estuaries of northeastern Brazil: A multi-component diversity approach. Ocean Coast. Manag. 143: 175-183. analysed the diversity of fish communities in estuarine complexes in Brazil and revealed differences between assemblages from Itapissuma, especially due to the relatively high abundance of some species of Gobiidae. The high abundance of gobiids in tropical estuaries may be partly due to their prolonged larval duration (Shen and Tzeng 2008Shen K., Tzeng W. 2008. Reproductive strategy and recruitment dynamics of amphidromous goby Sicyopterus japonicus as revealed by otolith microstructure. J. Fish Biol. 73: 2497-2512.), closely linked to the mainly muddy substrate and thus restricting their migrations to the sea (Vasconcelos Filho and Oliveira 1999Vasconcelos Filho A.L., Oliveira A.M.E. 1999. Composição e ecologia da ictiofauna do Canal de Santa Cruz (Itamaracá-PE, Brasil). Trab. Ocean. UFPE 27: 101-113.).

In the coastal environment of the IIC, the marine stragglers predominated in richness, abundance and biomass in all periods. However, the percentages of resident (estuarine) and dependent (marine migrant) species were also high, thus confirming the dependence between the estuary and coast of the IIC. The connection between continental and marine environments is an essential characteristic, as marine species are important exporters of energy to the adjacent coastal areas (Vasconcelos Filho et al. 2009Vasconcelos Filho A.L., Neumann-Leitão S., Eskinazi-Leça E., et al. 2009. Hábitos alimentares de consumidores primários da ictiofauna do sistema estuarino de Itamaracá (Pernambuco - Brasil). Rev. Bras. Eng. Pesca 4: 21-31.). Also, the coast of the IIC offers favourable conditions for the development of the marine fish fauna as protection and food resource (Medeiros et al. 2001Medeiros C., Kjerfve B., Araújo Filho M., et al. 2001. The Itamaracá Estuarine Ecosystem, Brazil. In: Seelinger U., Kjerfve B. (eds), Ecological Studies: Coastal Marine Ecosystems of Latin America. Springer-Verlag, New York, pp. 71-81.).

In relation to the feeding guild approach, our findings emphasized that the substrate of the IIC is of extreme importance for the high productivity in the system (CPRH 2010CPRH. Agência Estadual de Meio Ambiente. 2010. Diagnóstico Sócio ambiental da Área de Proteção Ambiental de Santa Cruz. Companhia Pernambucana de Meio Ambiente, Recife, 388 pp.), contributing to the high occurrence of species with feeding habits associated with the substrate (i.e. zoobenthivores and detritivores). The high availability of organic rich detritus in mangroves may increase the feeding opportunities for detritivores (Kuo et al. 1999Kuo S., Lin H., Shao K. 1999. Fish assemblages in the mangrove creeks of northern and southern Taiwan. Estuaries and Coasts 22: 1004-1015.), and can be considered the main trophic contribution factor for the estuarine fish fauna (Paiva et al. 2008Paiva A.C.G., Chaves P.D.T.D.C., Araújo M.E. 2008. Estrutura e organização trófica da ictiofauna de águas rasas em um estuário tropical. Rev. Bras. Zool. 25: 647-661.). In north Brazil, Loureiro et al. (2016)Loureiro S.N., Reis-Filho J.A., Giarrizzo T. 2016. Evidence for habitat-driven segregation of an estuarine fish assemblage. J. Fish Biol. 55: 804-820. observed that fish assemblage was strongly associated with substrates composed of organic matter. The high richness of zoobenthivores in the estuarine area of the IIC can be attributed to the great abundance of available benthic fauna (Silva 2013Silva A.M.C. 2013. Composição da meiofauna na ilha de Itamaracá e sua relação com a descrição morfoscópica e morfométrica dos grãos, Pernambuco. Rev. Nord. Zool. 7: 34-47.). Benthos is one of the structuring elements of the food web and plays an important role in the system dynamics (Herman et al. 1999Herman P.M.J., Middelburg J.J., van de Koppel J., et al. 1999. Ecology of Estuarine Macrobenthos. Adv. Ecol. Res. 29: 195-240.), transferring energy to fishes in estuarine environments (Buchheister and Latour 2015Buchheister A., Latour R.J. 2015. Diets and trophic-guild structure of a diverse fish assemblage in Chesapeake Bay, U.S.A. J. Fish Biol. 86: 967-992.). Detrivores dominated in abundance and biomass mainly due to large supply of organic matter and detritus in the IIC (Vasconcelos Filho et al. 2009Vasconcelos Filho A.L., Neumann-Leitão S., Eskinazi-Leça E., et al. 2009. Hábitos alimentares de consumidores primários da ictiofauna do sistema estuarino de Itamaracá (Pernambuco - Brasil). Rev. Bras. Eng. Pesca 4: 21-31., 2010Vasconcelos Filho A.L., Neumann-Leitão S., Eskinazi-Leça E., et al. 2010. Hábitos alimentares de peixes consumidores secundários do Canal de Santa Cruz, Pernambuco, Brasil. Trop. Oceanogr. 38: 121-128.), which support estuarine trophic webs (Hoffman et al. 2008Hoffman J.C., Bronk D.A., Olney J.E. 2008. Organic matter sources supporting lower food web production in the tidal freshwater portion of the York River estuary, Virginia. Estuaries and Coasts 31: 898-911.). The estuarine organic material of the IIC originates from various rivers (Eskinazi-Lessa et al. 1999Eskinazi-Leça E., Barros H.M., Macedo S.J. 1999. Estuarine management in northeastern Brazil: the estuarine complex of Itamaracá. Trans. Ecol. Environ. 27: 247-256.). The river discharge, sediment resuspension, mangrove litter, waste input, terrestrial runoff and atmospheric input are sources of nutrients in the IIC estuary (Medeiros 1991Medeiros C. 1991. Circulation and mixing processes in the Itamaracá estuarine system, Brazil. Ph.D. thesis, Univ. South Carolina, 131 pp.). The highest proportion of detritus usually occurs in environments with great amounts of organic matter. Detritus is consumed, constituting a link between organic production and animal nutrition, and increasing the efficiency of the energy transfer between the trophic levels (Qasim and Sankaranarayanan 1972Qasim S.Z., Sankaranarayanan V.N. 1972. Organic detritus of a tropical estuary. Mar. Biol. 15: 193-199.).

The large supply of zoobenthic fauna (Silva 2013Silva A.M.C. 2013. Composição da meiofauna na ilha de Itamaracá e sua relação com a descrição morfoscópica e morfométrica dos grãos, Pernambuco. Rev. Nord. Zool. 7: 34-47.) and the sandy substrate along the coast (Almeida and Manso 2011Almeida T.L.M., Manso V.A.V. 2011. Sedimentologia da plataforma interna adjacente a Ilha de Itamaracá - Pe. Est. Geol. 21: 135-152.) favour the high species richness and abundance of zoobenthivores in the IIC coastal area. Benthophagous fish are highly associated with sandy substrates (Loureiro et al. 2016Loureiro S.N., Reis-Filho J.A., Giarrizzo T. 2016. Evidence for habitat-driven segregation of an estuarine fish assemblage. J. Fish Biol. 55: 804-820.). The dominance of piscivores in biomass is mainly due to large carangids, which benefit from a high supply of food in the coastal area. Carangids are visual, active predators that spend a great part of their time on the reef searching for prey (Cervigón 1972Cervigón F. 1972. Los peces. In: Ginés H., Margalef R. (eds), Ecología Marina. Dossat S. A, Caracas, pp. 308-355.): they feed on fish and also consume benthic prey to complement their diets (Moreno-Sánchez et al. 2016Moreno-Sánchez X.G., Palacios-Salgado D.S., Abitia-Cárdenas L.A., et al. 2016. Importance of benthos in the trophic structure of the ichthyofauna of Los Frailes reef, Gulf of California, Mexico. In: Riosmena-Rodriguez R. (ed), Marine benthos: biology, ecosystem functions, and environmental impact. Nova Science Publishers, New York, pp. 1-37.).

Estuaries are dynamic ecosystems subject to notable variability of environmental conditions, and their fish assemblages show within-estuary seasonal and spatial variations, so taking into account this variability should further clarify trait patterns and drivers of estuarine fish (Henriques et al. 2017Henriques S., Guilhaumon F., Villéger S. 2017. Biogeographical region and environmental conditions drive functional traits of estuarine fish assemblages worldwide. Fish Fish. 18: 752-771.). The IIC is an important ecosystem for several species that inhabit or visit the area, mainly associated with the substrate. However, coastal areas are exposed to multiple anthropogenic pressures (Blaber and Barletta 2016Blaber S.J.M., Barletta M. 2016. A review of estuarine fish research in South America: what has been achieved and what is the future for sustainability and conservation? J. Fish Biol. 89: 537-568.) that can alter the structure and function of the fish community (Baptista et al. 2015Baptista J., Martinho F., Nyitrai D., et al. 2015. Long-term functional changes in an estuarine fish assemblage. Mar. Pollut. Bull. 97: 125-134.). The anthropogenic stresses and climate changes may facilitate or inhibite the processing of detritus and consequently cause dramatic shifts in species composition, which are often long-lasting and difficult to reverse (Ooi and Chong 2011Ooi A.L., Chong V.C. 2011. Larval fish assemblages in a tropical mangrove estuary and adjacent coastal waters: offshore-inshore flux of marine and estuarine species. Cont. Shelf Res. 31: 1599-1610.). The increase in human impacts could significantly affect the topology and functioning of the food web by altering stabilizing elements of the network and decreasing the diversity of trophic flows that ensures the resilience of the trophic structure (Lobry et al. 2008Lobry J., David V., Pasquaud S., et al. 2008. Diversity and stability of an estuarine trophic network. Mar. Ecol. Prog. Ser. 358: 13-25.). From the point of view of ecosystem management, it is necessary to identify and understand the biotic and abiotic effects on the distribution of fish fauna as a precursor for the management and monitoring of coastal environments (Pichler et al. 2017Pichler H.A., Gary C.A., Broadhurst M.K., et al. 2017. Seasonal and environmental influences on recruitment patterns and habitat usage among resident and transient fishes in a World Heritage Site subtropical estuary. J. Fish Biol. 90: 396-416.).

ACKNOWLEDGEMENTSTop

The first author thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the graduate scholarship and CNPq (Conselho Nacional de Desenvolvimento Científico) for the sandwich PhD scholarship. The last author also thanks CNPq for a research grant. The authors wish to thank the colleagues who assisted in the field and laboratory work. This work was financially supported by CAPES-COFECUB (Process 88881.142689/2017-01) and CNPq and the Instituto Nacional de Ciência e Tecnologia - Ambientes Marinhos Tropicais (CNPq Process 565054).

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SUPPLEMENTARY MATERIAL

The following supplementary material is available through the online version of this article and at the following link:
http://scimar.icm.csic.es/scimar/supplm/sm04855esm.pdf

Fig. S1. – Species accumulation curve of the estuary (A) and coast (B), computed by a random method without replacement. Mean species richness value ± SD.

Table S1. – Data collection dates according to the environmental and type of fishing gear utilised in the Itapissuma/Itamaracá Complex, northeastern Brazil.

Table S2. – Literature utilised for classication of the ecologic guilds of the ichthyofauna captured in the Itapissuma/Itamaracá Complex, northeastern Brazil. EUFG-Estuarine Use Functional Groups; FMFG-Feeding Mode Functional Groups, basead Elliott et al. (2007).