INTRODUCTION
Species abundance distribution has been a major theme in ecology since pivotal studies conducted in the 1940s (e.g. Fisher et al., Reference Fisher, Corbet and Williams1943; Preston, Reference Preston1948) and its theoretical and practical aspects remain central for understanding species' ecological roles (Dornelas et al., Reference Dornelas, Magurran, Buckland, Chao, Chazdon, Colwell, Curtis, Gaston, Gotelli, Kosnik, McGill, McCune, Morlon, Mumby, Øvreås, Studeny and Vellend2013; Shimadzu et al., Reference Shimadzu, Dornelas, Henderson and Magurran2013) and for biological conservation (Magurran & McGill, Reference Magurran and McGill2010). A key aspect when studying species abundance distribution is to understand how abiotic and biotic factors influence temporal variations in biological communities in different time scales (Blaber & Blaber, Reference Blaber and Blaber1980; Dornelas et al., Reference Dornelas, Magurran, Buckland, Chao, Chazdon, Colwell, Curtis, Gaston, Gotelli, Kosnik, McGill, McCune, Morlon, Mumby, Øvreås, Studeny and Vellend2013). On estuarine mudflats, short- and medium-time scales along the diel and seasonal cycles, respectively, may affect the population dynamics and the diversity of fish assemblages (Nagelkerken et al., Reference Nagelkerken, Blaber, Bouillon, Green, Haywood, Kirton, Meynecke, Pawlik, Penrose, Sasekumar and Somerfield2008). For instance, the seasonal variation in this estuarine habitat can be driven by fluctuations in environmental conditions and by biological factors such as fish recruitment, spawning patterns and trophic responses (Pessanha & Araújo, Reference Pessanha and Araújo2003; Pessanha et al., Reference Pessanha, Araújo, Azevedo and Gomes2003; Ribeiro et al., Reference Ribeiro, Bentes, Coelho, Gonçalves, Lino, Monteiro and Erzini2006; Castillo-Rivera et al., Reference Castillo-Rivera, Zárate-Hernández, Ortiz-Burgos and Zavala-Hurtado2010).
Short-term variations are particularly important for the dynamics of fish assemblages, especially in intertidal and immediate subtidal regions such as sandy beaches (Gibson et al., Reference Gibson, Robb, Burrows and Ansell1996; Godefroid et al., Reference Godefroid, Hofstaetter and Spach1998; Beyst et al., Reference Beyst, Vanaverbeke, Vincx and Mees2002; Gaelzer & Zalmon, Reference Gaelzer and Zalmon2008), reefs (Hobson, Reference Hobson1965), sheltered bays (Pessanha & Araújo, Reference Pessanha and Araújo2003; Pessanha et al., Reference Pessanha, Araújo, Azevedo and Gomes2003), coastal lagoons (Castillo-Rivera et al., Reference Castillo-Rivera, Moreno and Iniestra1994, Reference Castillo-Rivera, Montiel, Sanvicente-Añorve and Zárate2005a; Arceo-Carranza et al., Reference Arceo-Carranza, Vega-Cendejas and Santillana2013), coastal areas (Albert, Reference Albert1995; Soares & Vazzoler, Reference Soares and Vazzoler2001) and estuaries (Gray et al., Reference Gray, Chick and McElligott1998; Griffiths, Reference Griffiths2001; Methven et al., Reference Methven, Haedrich and Rose2001; Castillo-Rivera et al., Reference Castillo-Rivera, Zárate and Ortiz2005b, Reference Castillo-Rivera, Zárate-Hernández, Ortiz-Burgos and Zavala-Hurtado2010; Figueiredo & Vieira, Reference Figueiredo and Vieira2005; Ley & Halliday, Reference Ley and Halliday2007; Hagan & Able, Reference Hagan and Able2008; Becker et al., Reference Becker, Cowley, Whitfield, Järnegren and Næsje2011; Zárate-Hernández et al., Reference Zárate-Hernández, Castillo-Rivera, Sanvicente-Añorve and Ortiz-Burgos2012). These prior studies revealed that fish species have numerous strategies for dealing with short-term fluctuations, involving adaptation along the developmental stages, predator avoidances, feeding habits, swimming ability and mobility.
In tidal mudflats, environmental changes associated with photoperiod and tides are important factors affecting foraging activity of fish species and their ability to escape from predators (Pessanha & Araújo, Reference Pessanha and Araújo2003; Pessanha et al., Reference Pessanha, Araújo, Azevedo and Gomes2003). The partition of the temporal niche along the day/night cycle, for instance, is considered to be a mechanism leading to reduced competition among fish species in shallow waters for food and space resources (Kronfeld-Schor & Dayan, Reference Kronfeld-Schor and Dayan2003). Indeed, inter- and intraspecific changes along the diel cycle are common in many species (Alanara et al., Reference Alanara, Burns and Metcalfe2001; Kronfeld-Schor & Dayan, Reference Kronfeld-Schor and Dayan2003). Coupled with the population dynamics, these factors can result in changes in fish assemblage attributes, such as abundance and species richness, along the diel cycle (Gibson et al., Reference Gibson, Robb, Burrows and Ansell1996; Morrisson et al., Reference Morrisson, Francis, Hartill and Parkinson2002; Ribeiro et al., Reference Ribeiro, Bentes, Coelho, Gonçalves, Lino, Monteiro and Erzini2006). Despite their recognized ecological importance as recruitment areas for fish fauna in many estuaries (Kennish, Reference Kennish1990; Beck et al., Reference Beck, Heck, Able, Childers, Eggleston, Gillanders, Halpern, Hays, Hoshino, Minello, Orth, Sheridan and Weinstein2001), tidal mudflats remain poorly studied with respect to the influence of temporal variations in abiotic factors on the fish fauna (Morrisson et al., Reference Morrisson, Francis, Hartill and Parkinson2002; Godefroid et al., Reference Godefroid, Spach, Schwarz, Queiroz and Oliveira Neto2003). The present study investigates temporal variations on fish assemblages based on the hypothesis that fishes co-occurring in the same habitat have different patterns of temporal segregation at short- and medium scales that optimize resource use and habitat partitioning. To evaluate this hypothesis, we analysed temporal variations in fish assemblage attributes (e.g. abundance, biomass and species richness) in a tropical estuarine mudflat and their correlations with season, photoperiod and tidal cycle.
MATERIALS AND METHODS
Study area
The study was carried out at the Mamanguape River estuary, which is located on the north coast of the Paraíba state in north-east Brazil and extends for 25 km in length (east-west direction) and for 5 km in breadth (north-south direction). It is part of the Environmental Protection Area of Barra de Mamanguape (Figure 1). The regional climate is classified as hot and humid (Köppen's AS). The wet season begins in February and lasts until July, with maximum rainfall occurring from April to June, whereas the dry season occurs from August to January, with the lowest rainfall occurring between October and December (Pereira & Alves, Reference Pereira and Alves2006). The mean rainfall recorded in the area is between 1750 and 2000 mm annually, and the mean temperature is 24–26°C. There is a well-preserved mangrove in the area, composed of Avicennia germinans, Avicennia schaueriana, Conocarpus erectus, Laguncularia racemosa and Rhizophora mangle, which grows around the primary channel and tidal creek and extends to 6 km2, in addition to Atlantic Forest remnants (Rocha et al., Reference Rocha, Mourão, Souto, Barboza and Alves2008). Endangered species, such as the seahorse, Hippocampus reidi, and the West Indian manatee, Trichechus manatus, are also found in this estuary (Mourão & Nordi, Reference Mourão and Nordi2003; Castro et al., Reference Castro, Diniz, Martins, Vendel, Oliveira and Rosa2008).
Estuary of the Mamanguape River (Paraíba state, Brazil) located in the mouth of the Tinto River, with the location of the studied tidal flat.
The Curva do Pontal beach (6°46′27″S 34°55′20″W) is a tidal mudflat located 2.3 km from the estuary mouth, is 1200 m long and has very calm waters because of the diminished influence of waves (Figure 1). The tidal mudflat is greatly influenced by the entrance of ocean waters, where marine sediments are regularly exposed and submerged by tidal action, and has a maximum depth of 4 m. The tidal mudflat examined is a non-vegetated area with a gentle slope and fine muddy sediment in the intertidal zone, whereas in the subtidal zone, seagrass, sessile invertebrates, macroalgae, mangrove leaves and fallen branches form the benthic cover (Xavier et al., Reference Xavier, Cordeiro, Tenório, Diniz, Júnior, Rosa and Rosa2012).
Fish collections and sample processing
Field samplings were carried out over the hydrological regime, with three field surveys conducted monthly in 2012 in wet (May, June and July) and dry (October, November and December) seasons. The fish were sampled using a beach seine (10.0 × 1.5 m; 8 mm mesh size) and each seine haul was 30 m long and was carried parallel to the shore at depths of ~1.5 m. Each haul covered an area of ~30 m2. This procedure was replicated three times on each sampling occasion. Temperature and salinity were measured, using a thermometer and an optical refractometer, respectively. The total length (TL, mm) and body weight (g) were measured for each individual fish. In order to evaluate the fluctuations in fish assemblage attributes along the 24 h cycle, samples were taken in the following photoperiods: at 1 h before sunrise (DAW: dawn), 1 h after sunrise (MOR: morning), midday (MDA), afternoon (AFT), 1 h before sunset (DUS: dusk), 1 h after sunset (EVE: evening), midnight (MNI) and late night (LNI). In order to investigate the influence of the tidal regime, fish sampling was conducted at the high and low tides. In the study area, tidal oscillation along the 24 h cycle is characterized by two peaks of high and low tides during daytime and another two peaks of high and low tides at the night-time. Samples taken during the high tide (MOR, DUS, EVE and DAW) were pooled as high tide, whereas those collected at low tide (MDA, AFT, MNI and LNI) were pooled as low tide.
Data analyses
Permutational multivariate analysis of variance (PERMANOVA) was used to test the null hypothesis that there were no changes in abiotic factors (salinity and temperature) and in fish assemblage attributes in relation to the season, photoperiod and tidal cycles. Each abiotic (salinity and temperature) and biological (CPUE, biomass, species richness and evenness) data matrix was initially fourth root transformed and used to produce a resemblance matrix using the Bray–Curtis similarity measure. Pair-wise test comparisons were used to determine which groups differed within factors based on 9999 permutations performed for each test. Evenness was computed as the Hill (E5) index (Magurran, Reference Magurran2005).
Principal Components Ordinations (PCO) were used to examine short- and medium-scale variations in fish assemblage according to season (dry or wet), photoperiod (DAW, MOR, MDA, AFT, DUS, EVE, MNI and LNI) and tidal (lower and higher) cycles. Rare species in the fish species matrix were downweighted in order to prevent them from having an excessive influence on the multivariate analysis. We defined rare species as those represented by less than 30 individuals caught in each photoperiod. Similarity percentages (SIMPER) were also calculated to determine which species contributed to changes in assemblage data (PRIMER 6 + PERMANOVA, 2006) (Clarke & Gorley, Reference Clarke and Gorley2001; Anderson et al., Reference Anderson, Gorley and Clarke2008).
RESULTS
Environmental factors
Overall, the analysis of the environmental factors revealed lower variation and no statistically significant differences in temperature when compared with salinity. Higher mean temperature values were observed at midday (MDA) both in the dry (30°C ± 0.46) and in the wet (29°C ± 0.54) season (Figure 2). However, these seasonal variations in temperature were not statistically significantly different for either season (Pseudo-F 1.143 = 2.1846; P = 0.1364) or photoperiod (Pseudo-F 7.143 = 0.7436; P = 0.6889), and also for the interaction between them (Pseudo-F 7.143 = 0.5043; P = 0.8540). Mean salinity values were higher during dusk (DUS) in the dry season (35.9 ± 2.2) and morning (MOR) of the wet (33.6 ± 3.3) period (Figure 2). The PERMANOVA tests showed significant differences in mean values along the season (Pseudo-F 1.143 = 50.277; P = 0.0001) and photoperiod cycles (Pseudo-F 7.143 = 3.6992; P = 0.0013), and also for the interaction between these two factors (Pseudo-F 7.143 = 3.5079; P = 0.0019). Pair-wise tests showed that salinity was significantly different among photoperiod phases in both the wet and dry seasons (Table 1). In addition, higher variation was observed among mean salinity values in the wet than in the dry season (Figure 2, Table 1).
Mean values (±95% CI) of temperature (A, °C) and salinity (B) along the photoperiod (MOR: morning; MDA: midday; AFT: afternoon; DUS: dusk; EVE: evening; MNI: midnight; LNI: late night; DAW: dawn) in the tidal flat of the Mamanguape River during wet and dry seasons. White and dark bars below the x axis denote the diurnal and nocturnal periods, respectively.
Results of the PERMANOVA pair-wise test to the mean salinity values along the photoperiod during the wet and dry periods in the tidal flat of the Mamanguape River.
MOR: morning; MDA: midday; AFT: afternoon; DUS: dusk; EVE: evening; MNI: midnight; LNI: late night; DAW: dawn.
Asterisks denote statistically significant differences (P < 0.05).
Species composition and overall abundance patterns
A total of 6222 individuals representing 66 fish species (26 families) were collected (Supplementary Table S1). The family Engraulidae had the greatest number of species (eight), followed by Gerreidae and Gobiidae (six species each), and Mugilidae and Sciaenidae (five species each). Rhinosardinia bahiensis, Lycengraulis grossidens, Eucinostomus melanopterus, Atherinella brasiliensis, Ctenogobius boleosoma, Hyporhamphus unifasciatus and Mugil liza were the seven most abundant species, accounting for 75.3% of the total numerical abundance. In terms of biomass, Sphoeroides testudineus, R. bahiensis, L. grossidens, A. brasiliensis and H. unifasciatus were the most important species, representing 67.7% out of the total 21,338 g of fish collected.
Medium-term (seasonal) variations in fish assemblages
A greater number of individuals and species were captured in the wet than in the dry seasons (3138 and 60 vs 3084 and 52, respectively) (Supplementary Table S1). In the wet season, E. melanopterus, R. bahiensis, C. boleosoma, A. brasiliensis, M. liza and H. unifasciatus accounted for 70.6%, whereas in the dry season, only two species (R. bahiensis and L. grossidens) totalled 69.3% of the total numerical abundance. Biomass showed an opposite pattern, with higher values during the dry period. Fourteen species were caught exclusively in the wet season and 15 were found exclusively at the dry season (Supplementary Table S1). According to the PERMANOVA, biomass and numerical abundance (CPUE) showed statistically significant variation in their mean values in relation to season. CPUE, species richness and evenness (E) were higher during the wet season, whereas higher values of biomass were observed in the dry season (Table 2).
Results of the PERMANOVA tests for the variations in abundance (CPUE), biomass, species richness and evenness (E5-Hill) of the fish assemblages for the season (SEA), photoperiod (PHO) and tidal (TID) factors.
df, degrees of freedom; 9999 permutations; *significant values (P ≤ 0.05).
Principal Components Ordinations plot (PCO) revealed distinct groups of fish samples, contrasting wet and dry seasons, and explained 55.5% of total variance (Figure 3). Species characteristics of the dry season included E. melanopterus, M. liza, C. boleosoma and A. brasiliensis, whereas species more characteristic of the wet season included R. bahiensis, L. grossidens and C. macrops. Results of SIMPER analysis indicated that E. melanopterus, A. brasiliensis and C. boleosoma contributed mostly to similarities in the wet season (36.54%), whereas A. brasiliensis, L. grossidens and R. bahiensis were the major species responsible for the similarity in the dry season (28.62%) (Figure 3).
Principal Components Ordinations (PCO) plot of the individual abundance samples of fish assemblages captured in the tidal flat of the Mamanguape River considering the season, photoperiod and tide regime factors.
Short-term (photoperiod and tidal regime) variations in fish assemblages
Overall, a higher number of individuals (54.8 ind haul−1) and biomass (31.08 g haul−1) were collected during the day, and only species number (7.4 species haul−1) was higher at night. Eight species were recorded exclusively during the day and 17 species were captured only at night (Supplementary Table S1). The PERMANOVA test showed statistically significant differences for all descriptors (CPUE, biomass, species richness and evenness) of the fish assemblage. CPUE and biomass were higher at midday (MDA) and afternoon (AFT), whereas species richness was higher at midday (MDA) and late night (LNI). The evenness was higher during morning (MOR) and evening (EVE) (Table 3).
Similarity values obtained by the SIMPER analysis among pair-wise periods along the photoperiod.
MOR: morning; MDA: midday; AFT: afternoon; DUS: dusk; EVE: evening; MNI: midnight; LNI: late night; DAW: dawn.
The PCO plot revealed distinct groups of fish samples and explained 55.5% of the total variance. The PCO plot showed a separation of diurnal from nocturnal samples (Figure 3). Species characteristic during the day included R. bahiensis, L. grossidens, E. melanopterus and M. liza, whereas those commonly found at night included A. brasiliensis, C. boleosoma and C. macrops. Table 3 shows the species that most contributed to differences along the periods of the photoperiod according to SIMPER.
There was an overall trend of higher fish abundance at low vs high tide (N = 3316 and N = 2906, respectively). However, higher species richness and biomass were recorded at high than at low tide (64 and 10,784.51 g vs 58 and 10,554.5 g, respectively). The dominant fishes at high tide were R. bahiensis, E. melanopterus, A. brasiliensis, L. grossidens, H. unifasciatus, C. boleosoma, Anchoviella lepidentostole, C. macrops and A. brevirostris, whereas at low tide dominated L. grossidens, R. bahiensis, E. melanopterus, M. liza, C. boleosoma, A. brasiliensis, H. unifasciatus, G. stomatus, Sphoeroides greeleyi, S. testudineus and Anchoa marinii. An additional eight fish species were caught only at high tide, whereas eight different species were caught only during low tide (Supplementary Table S1).
Mean values of abundance varied along the tidal cycle, with statistically significant higher values at low tide. The mean values of biomass showed an opposite pattern, with statistically significant higher values at high tide. The species richness and evenness showed similar values between high and low tide with no statistically significant differences (Table 2). Results of SIMPER analysis showed that A. brasiliensis, E. melanopterus, R. bahiensis and L. grossidens had a greatest contribution to similarities during high tide (27.12%) and A. brasiliensis, E. melanopterus, L. grossidens, C. boleosoma and R. bahiensis were the major species responsible for the similarity in the lower tide (22.82%). The PCO plot did not show a clear segregation between samples obtained at the high and low tides (Figure 3).
Fish variations and multiple interactions with environmental factors
Biomass and species richness, and to a lesser extent CPUE and evenness, showed statistically significant interactions with season, photoperiod and tidal factors (Table 2), revealing a mutual dependency and interaction of these attributes with short- and medium-term scales (Figure 4). For instance, biomass tended to be higher during the dry season and its temporal oscillation along the tidal cycles had distinct patterns along the photoperiod in each season. During the wet season, biomass differences between low and high tides were less pronounced than during the dry season, which showed two distinct patterns along the photoperiod (higher biomass during midday and afternoon and an opposite pattern at midnight/late night). A similar interaction was also observed for species richness, which showed distinct patterns between high and low tides along the photoperiod at each season (Figure 4). Although not displaying significant three-factor interaction, CPUE response showed statistically significant interactions between season and photoperiod, and photoperiod and tidal regime. Among all factors, evenness was the only one showing no interactions, with its temporal variation associated exclusively with photoperiod (Table 2).
Mean (±95% CI) values of CPUE (individuals per haul), biomass (g), species richness (S) and evenness (E) of fish assemblages caught in the tidal flat of the Mamanguape River at high (dashed lines) and low (continuous lines) tides along the photoperiod for the wet and dry seasons. Codes for photoperiod are: MOR: morning; MDA: midday; AFT: afternoon; DUS: dusk; EVE: evening; MNI: midnight; LNI: late night; DAW: dawn.
DISCUSSION
We showed that temporal changes in important attributes of a mudflat fish assemblage, such as biomass, numerical abundance and species richness, correlate with environmental factors occurring at short- and medium-term temporal scales. In some instances, observed day–night differences in abundance and diversity seemed to result from highly abundant species belonging to families like Engraulidae, Clupeidae, Mugilidae, Hemiramphidae and Gerreidae. In contrast, higher species richness at night could be related to a greater number of more predatory fish exhibiting solitary swimming behaviour (single-species), such as Gymnothorax ocellatus, Myrichthys ocellatus, Ophichthus parilis, Strongylura marina, S. timucu and Cynoscion leiarchus, which usually move into shallower waters (Girsa & Zhuravel, Reference Girsa and Zhuravel1983; Gibson et al., Reference Gibson, Robb, Burrows and Ansell1996). A similar pattern was found by Hobson (Reference Hobson1965) who first described species of the families Pomadasyidae, Carangidae and Sciaenidae active at night in coral reefs.
As constraints for diel variation, important conditions include obtaining food or rest, the avoidance of adverse physicochemical conditions and, moreover, the behaviour to shelter against predators (Gibson et al., Reference Gibson, Robb, Burrows and Ansell1996, Reference Gibson, Pihl, Burrows, Modin, Wennhage and Nickell1998; Morrisson et al., Reference Morrisson, Francis, Hartill and Parkinson2002). In fish ecology, one of the main factors that is invoked to explain the high density of fish species in shallow water habitats are features related with their trophic ecology, in which diurnal species have been characterized as filter-feeding or zoobenthivorous. In the present study, Engraulidae, Clupeidae and Gerreidae were recorded in high abundance during the day, because fish species in these families are usually visual predators and environmental light conditions represent a key factor in their feeding success (Reis & Dean, Reference Reis and Dean1981; Kerschner et al., Reference Kerschner, Peterson and Gilmore1985; Castillo-Rivera et al., Reference Castillo-Rivera, Montiel, Sanvicente-Añorve and Zárate2005a). In some systems, there is a strong diel influence, with higher abundance of dominant species in the day as, for instance, in beaches (Layman, Reference Layman2000; Pessanha & Araújo, Reference Pessanha and Araújo2003), bays (Nagelkerken et al., Reference Nagelkerken, Dorenbosch, Verberk, Moriniere and Velde2000) and estuaries (Castillo-Rivera et al., Reference Castillo-Rivera, Zárate-Hernández, Ortiz-Burgos and Zavala-Hurtado2010).
Another factor that could be related to the observed differences between day and night is the ability of net avoidance by fish. This characteristic has been recorded with greater evidence during the day because the fish would visually detect the presence of a fishing net (Rozas & Minello, Reference Rozas and Minello1997). However, this mechanism probably would be of little influence on the studied tidal flat, due to the low transparency (on mean <35 cm) recorded at this site. According to Morrisson et al. (Reference Morrisson, Francis, Hartill and Parkinson2002), such influence is unlikely in areas with turbid waters. Furthermore, the highest abundance was recorded during daylight, which seems to refute this hypothesis.
Abundance differences in the shorter temporal scale of photoperiod were also observed in the present study and they are usually attributed to factors directly or indirectly related to foraging activity (Rountree & Able, Reference Rountree and Able1993; Nagelkerken et al., Reference Nagelkerken, Dorenbosch, Verberk, Moriniere and Velde2000; Pessanha & Araújo, Reference Pessanha and Araújo2003; Madurell et al., Reference Madurell, Cartes and Labropoulou2004; Hagan & Able, Reference Hagan and Able2008) and behavioural responses to avoid predators (Layman, Reference Layman2000; Pessanha et al., Reference Pessanha, Araújo, Azevedo and Gomes2003). On some occasions, we observed higher abundance of R. bahiensis, L. grossidens and E. melanopterus at midday in the mudflat and they were explained by the presence of pelagic species (with the exception of E. melanopterus), which usually forms mixed-species schools (Whitehead, Reference Whitehead1985; Whitehead et al., Reference Whitehead, Nelson and Wongratana1988; Helfman et al., Reference Helfman, Collette, Facey and Bowen2009). At late night, despite the lower influence of R. bahiensis and E. melanopterus, there was the contribution of typical species of the intertidal zone such as C. boleosoma and S. tessellatus, which are more associated with muddy substrates (Nelson, Reference Nelson2006; Helfman et al., Reference Helfman, Collette, Facey and Bowen2009). Diel microhabitat partitioning by estuarine fishes is common as a result of size-related differences in feeding efficiency or predator avoidance (Rountree & Able, Reference Rountree and Able1997). Small-scale movements within a nursery could further enhance the survival and growth of juvenile fishes (Gibson et al., Reference Gibson, Pihl, Burrows, Modin, Wennhage and Nickell1998).
The highest species richness recorded at midnight and late night in some occasions was probably due to the movement of fully marine species and reef fishes (A. surinamensis, S. brasiliensis and S. marina, S. timucu), which are typical predatory species that might enter the mudflat to prey upon juvenile fish (Hobson, Reference Hobson1965; Castillo-Rivera et al., Reference Castillo-Rivera, Zárate-Hernández, Ortiz-Burgos and Zavala-Hurtado2010). This hypothesis seems to be corroborated by the fact that the studied tidal flat is located adjacent to the estuary and a few kilometres from a sandstone reef. Fish of the families Haemulidae and Lutjanidae have been shown to undertake daily feeding migrations that are often precisely timed and occur along established routes (Nagelkerken et al., Reference Nagelkerken, Dorenbosch, Verberk, Moriniere and Velde2000; Morrisson et al., Reference Morrisson, Francis, Hartill and Parkinson2002). Estuarine species such as T. nattereri and H. roberti, which are characterized by a carnivorous diet, also contributed to this high species richness during the night. Such an increase in predators in the shallow water at night is probably related to an increase in biomass at night; a similar pattern had been described for other systems such as beaches (Pessanha et al., Reference Pessanha, Araújo, Azevedo and Gomes2003; Vasconcellos et al., Reference Vasconcellos, Araújo, Santos and Silva2010), estuaries (Ley & Halliday, Reference Ley and Halliday2007) and seagrass beds (Kwak et al., Reference Kwak, Hwang, Han, Kim and Huh2011).
The twilight hours (dusk and dawn) tended to show higher evenness, probably due to events described by Hobson (Reference Hobson1965), when diurnal and nocturnal groups essentially replace one another ecologically. The light intensity during the dusk and dawn serves as indicators of changes in environmental conditions that influence the behaviour of fish of different trophic groups (Manteifel et al., Reference Manteifel, Girsa, Pavlov and Thorpe1978). In tropical mudflats, crepuscular predators include jacks (C. latus) and snappers (Lutjanus synagris), but also smaller species such as gobies (C. boleosoma and G. stomatus) and flatfishes (C. macrops, C. spilopterus and Symphurus tessellatus). However, some of the largest shoals of fishes encountered by day in tropical waters, specifically during the hour preceding dusk, move to the bottom and rest in relatively exposed locations at night, such as herrings (R. bahiensis), silversides (A. brasiliensis) and anchovies (L. grossidens, A. lepidentostole, A. marinii), and they leave this area at dawn.
Although less apparent than those changes in fish assemblage attributes observed at finer temporal scales (day–night and photoperiod), there were changes along the tidal cycle as well. For instance, higher abundance and species richness were often recorded at low tide, probably due to a greater representation of the fish samples of different trophic guilds, such as detritivores (M. liza), omnivores (C. boleosoma), herbivores (G. stomatus) and benthivores (S. greeleyi, S. testudineus). Prior works have pointed out that tidal influence in mudflats affects not only the distribution, but also the behavioural and feeding patterns of fish (Rozas & Minello, Reference Rozas and Minello1997; Favaro et al., Reference Favaro, Lopes and Spach2003; Nybakken & Bertness, Reference Nybakken and Bertness2004). Moreover, during low tide there was a greater proportion in the samples of estuarine residents who are associated closely with the substrate (flounder, puffers and gobies), in contrast to the stronger influence of pelagic fish during high tide, who usually move up to the upper portion of the mudflat as water level rises (Rozas & Minello, Reference Rozas and Minello1997; Reis-Filho et al., Reference Reis-Filho, Nunes, Menezes and Souza2010).
Changes in fish assemblage attributes were also observed at the coarser temporal scale of wet and dry seasons, which are typical of tropical latitudes (Lowe-McConnell, Reference Lowe-McConnell1987). In the wet season, there was a greater number of juveniles of A. marinii, M. curema, M. liza, H. unifasciatus, L. synagris, E. melanopterus and larvae of A. brevirostris and A. lepidentostole. In contrast, there was a prevalence of juvenile individuals of L. grossidens in the dry season. This pattern coincided with higher species richness and a greater variety of trophic guilds during the wet season, such as omnivorous, zooplanktivorous, benthivorous and detritivorous. This finding could be related with greater input of allochthonous food resources into the mudflat. Overall, higher rainfall in tropical latitudes is associated with an increase in primary productivity and input of allochthonous organic matter (detritus) and nutrients carried out by increased freshwater discharge, which leads to higher food availability (Junk et al., Reference Junk, Bayley and Sparks1989). It seems plausible to hypothesize that an increase in food resources in the wet season would favour a higher abundance of juvenile fishes and greater diversity of trophic guilds in the studied mudflat. This hypothesis is well investigated in tropical rivers (e.g. Winemiller, Reference Winemiller1990), but much less evidence is available for tropical estuaries (e.g. Livingston et al., Reference Livingston, Niu, Lewis and Woodsum1997; Castillo-Rivera et al., Reference Castillo-Rivera, Zárate-Hernández, Ortiz-Burgos and Zavala-Hurtado2010). Future field studies would be necessary to evaluate if this mechanism also drives food web dynamics at tropical estuaries.
The dry season had lower fish abundance and biomass was nearly 50% lower than the wet season due to the greater number of young-of-the-year of A. vulpes, A. brevirostris, A. lepidentostole, S. guachancho, A. filifera, A. tricolor and E. melanopterus. Studies elsewhere have also reported the use of shallow waters by larvae and young-of-the-year (Blaber & Blaber, Reference Blaber and Blaber1980; Paterson & Whitfield, Reference Paterson and Whitfield2000), which is usually explained by the assumption that shallow-water habitats in estuaries provide abundant food and protection against predators (Pessanha et al., Reference Pessanha, Araújo, Azevedo and Gomes2000; Methven et al., Reference Methven, Haedrich and Rose2001; Potter et al., Reference Potter, Bird, Claridge, Clarke, Hyndes and Newton2001; Morrisson et al., Reference Morrisson, Francis, Hartill and Parkinson2002; Pessanha & Araújo, Reference Pessanha and Araújo2003). Therefore, the entrance of young-of-the-year and juvenile fish into shallow waters of the mudflat and their subsequent displacement into deeper waters after achieving greater body size and becoming adults could also be another mechanism leading to the observed seasonality in fish attributes like abundance and diversity.
In conclusion, our study revealed that fish fauna in a tropical tidal mudflat have complex responses to short- and medium-term temporal variations associated with hydrological (wet and dry seasons), tidal (low and high tides) and diel (24 h cycle) factors. Moreover, these complex responses and interactions vary according to the assemblage attribute being analysed, with significant temporal variations in biomass and species richness. Shorter-term variations on fish assemblages attributes were associated mainly with photoperiod and, to a lesser extent, to tidal range influence. In contrast, medium-term scale changes in fish abundance and species richness could be related with seasonality in recruitment patterns and higher availability of allochthonous food resources during the wet season. Future studies on the trophic ecology of these species will be useful to assess the role of these factors as determinants of diel changes, and also the possible role of this mudflat as a nursery area for some of these species.
SUPPLEMENTARY MATERIAL
The supplementary material for this article can be found at https://doi.org/10.1017/S0025315417001199
ACKNOWLEDGEMENTS
We are grateful to several colleagues in the Ichthyology Lab of the Universidade Estadual da Paraiba who helped in the fish collections and sample processing and Joseline Molozzi for helping with the data analyses.
FINANCIAL SUPPORT
This work was partially supported by the National System of Research on Biodiversity (SISBIOTA/BRASIL) and CNPq - Brazilian National Agency for Scientific and Technological Development (Proc. 563202/2010-6 and Proc. 477663), SISBIO gave permission to carry out the research in the protected area (Proc. 24557).
