Effects of a Red Tide on the Structure of Estuarine Fish Assemblages in Northeastern Brazil

Internat. Rev. Hydrobiol. 97 2012 5 389–404

DOI: 10.1002/iroh.201101457

JOSÉ AMORIM REIS-FILHO*, 1, 2, EDUARDO M. DA SILVA1, JOSÉ DE ANCHIETA CINTRA DA COSTA NUNES3 and FRANCISCO BARROS3

1Instituto de Biologia, Universidade Federal da Bahia, Campus de Ondina – 40170-115 Salvador, BA, Brazil; e-mail: [email protected]. 2ICHTUS Soluções em Meio Ambiente Ltda, Rua Frederico Simões, Nº 513 Ed. Orlando Gomes, Sala 211, 41820-774, Salvador, BA, Brazil 3Laboratório de Ecologia Bentônica – Instituto de Biologia, Universidade Federal da Bahia, Campus de Ondina, 40170-115 Salvador, BA, Brazil

Research Paper

Effects of a red tide on the structure of estuarine fish assemblages in northeastern Brazil

key words: Akashiwo sanguinea, fish mortality, red tide, Todos os Santos Bay

Abstract

The present study evaluated changes in an estuarine fish community caused by blooms of the dinoflagellate Akashiwo sanguinea. Samples were collected before, during and after the red tide using seine nets and surface and bottom nets in three areas near the affected area. The area was around the mouth of the Paraguaçu River. A total of 144 samples were collected, containing 1,989 individuals, with a total weight of 51.4 kg, belonging to 42 species in 29 families. During the red tide, fish density, richness and biomass decreased significantly. Atherinella brasiliensis and Sphoeroides greeleyi were the most abundant species during the red tide, indicating some possible resistance to the effects of the red tide. One month after the red tide, there was a rapid recovery of the density, biomass and richness of fish, and Cetengraulis edentulus was the most captured species. An important result of the present study is the finding that the dynamics of small populations of fish are often influenced by fortuitous events, and stochasticity may dominate. The establishment of a continuous and adequate monitoring program in the area may contribute to understanding the effects of red tides on fish population dynamics.

1. Introduction

Algal bloom events are characterized by the proliferation and occasional dominance of particular species which, in some cases, show an increase in their abundance to the point that their pigments change the color of the water, leading to the use of the term “red tide” (ANDERSON, 2009). Harmful algal blooms (HAB) are increasing in frequency and magnitude worldwide as a result of changes in the oceanic climate, increased coastal eutrophication and enhanced long-distance dispersal in ballast water (LANDSBERG, 2002; HEISLER et al., 2008; RABALAIS et al., 2009). The occurrence of HAB is associated with large loads of organic material and toxins that generally affect co-occurring organisms and the dynamics of marine food webs (ANDERSON, 2009) on different scales (LANDSBERG, 2002; GRANÉLI and TURNER, 2008).

* Corresponding author

A few decades ago, relatively few countries were affected by these blooms (SMITH, 1975; ANDERSON, 1989; GUZMÁN et al., 1990; HALLEGRAEFF, 1993), but many coastal countries are now affected, and large geographic areas may be impacted (LANDSBERG, 2002; GRANÉLI and TURNER, 2008; RICHLEN et al., 2010). Negative impacts, such as fish mortality, are one of several possible consequences of red tides (OKAICHI, 1997; VOGELBEIN et al., 2002; RICH- LEN et al., 2010) and have been observed in estuarine areas (BURKHOLDER et al., 1992; BURK- HOLDER et al., 1999; TANGO et al., 2006). Fish mortality events have increased considerably in recent years, typically as a result of the transfer of toxins to the food web (HALLEGRAEFF, 1993; HORNER et al., 1997; CEMBELLA et al., 2000). Other ways in which red tides can affect fish fauna are through excessive increases in plankton biomass (ANDERSON, 2009), localized anoxia (ANDERSON et al., 2002) and predation (VOLGELBEIN et al., 2002). Some non-toxic blooms can quickly increase oxygen consumption to levels that are lethal for fish survival, or may cause clogging of the gills owing to the accumulation of phytoplankton cells and possibly mucous (HORNER, 2002; GRANÉLI and TURNER, 2008). Due to these characteristics, HAB are likely to affect a much wider variety of taxa than other disturbances in marine ecosystems (PRATCHETT et al., 2008; BAUMAN et al., 2010). However, the effects of HAB on the structure of fish assemblages at small scales have not yet been studied. Red tides have caused major impacts on coastal economies (ANDERSON, 2009). Public perception of harmful algal blooms has the potential to impose significant economic losses on coastal regions. Loss of the use of recreational resources, lost tourism revenues, decreased consumption of seafood, lost ﬁshing time due to area closures, possible medical costs for treatment, and increased regulation on industries all represent decreases in economic welfare (WHITEHEAD et al., 2003). For instance, in China in 1989, more than US$ 40 million was spent in Hebei Province in response to the mortality of fish due to red tide events (WANG and LI, 1998). Between 1987 and 2000, the USA spent approximately US$ 775 million on remediation and monitoring (HOAGLAND and SCATASTA, 2006). Along the Maryland coast of the Chesapeake Bay, a 1997 bloom of algae resulted in fish kills, primarily of menhaden Brevoortia tyrannus (WHITEHEAD et al., 2003). In these cases, the dinoflagellates Pfiesteria piscicida and P. shumwayae were the cause of mortality, owing to toxin production, as has been well documented by GLASGOW et al., 2001; BURKHOLDER et al., 2005; and MOEL- LER et al., 2007. In Japan, approximately US$ 10 million are spent annually on the impacts of red tides on aquaculture and marine fisheries (OKAICHI, 1997), and in 2007, South Korea lost approximately US$ 11 million associated with the mortality of marine fish (NFRDI, 2008). However, monetary losses are normally underestimated (KAHN and ROCKEL, 1988). Coastal marine communities are being increasingly affected by disturbance events (MCCLANAHAN, 2002; THOMPSON et al., 2002), and fish communities might show resilience to events such as climate change and overfishing (PERRY et al., 2010). A red tide event can alter the resilience of some organisms (LANDSBERG, 2002). Nevertheless, to the best of our knowledge, no study that aimed to verify the impacts of HAB on the structure of fish assemblages on small scales has been reported. ANDERSON (2009) suggested that there is an enormous difficulty in regulating or controlling the effects of HAB because of a lack of research on all aspects of these events, including ecology, physiology and oceanography. In early March 2007, high fish mortality was reported in the western part of Todos os Santos Bay (TSB). Fish died continuously for approximately three weeks, and unofficial reports in the press indicated a total of 50 Mg of dead fish during this period. Water samples collected by the Bahia State Environmental Office (BAHIA, 2007), near the fish mortality sites throughout the duration of the event, did not show any abnormal values for organic substances, PAH or metals, indicating some other factor as the cause of the high fish mortality. Subsequent sampling indicated that a bloom of the dinoflagellate Akashiwo sanguinea (HIRASAKA) HANSEN et MOESTRUP was the cause of this event. Hence, the main objective of the present study was to evaluate the effects of the HAB on the composition, abundance and diversity of fish assemblages.

2. Materials and Methods

2.1. Study Area

The study area is located near the mouth of the Paraguaçu River, in the western part of TSB, which forms the largest estuarine complex of this bay (for further information on the location, refer to HATJE and ANDRADE, 2009). The affected area covered approximately 84 km2, and a maximum density of 3 million cells/L of the A. sanguinea was found (BAHIA, 2007). Three areas were sampled at the mouth of the Paraguaçu estuary (Fig. 1) due to their distinctive environmental characteristics. Area 1, located to the north of the mouth, exhibits many rocky reefs and mud flats, high hydrodynamics (high energy) and depths ranging from 1 to 6 m. Area 2, located in a tidal flat in Barra do Paraguaçu (just below the mouth), presents sandy-muddy sediments with reduced hydrodynamics (low energy) in the tidal flat and depths ranging from 0.6 to 27 m in the channel of the mouth. Finally, area 3 shows characteristics similar to area 2, differing only in its sediment composition, which is composed of a mixture of ter- rigenous and biogenic material carried by the river and by tides, associated with wide coverage of a mussel, Brachidontes exustus.

Figure 1. Location of the area affected by the red tide (dotted line gray) and the sampling sites (indicated by arrows). The isobaths of the study areas are shown in the inserted figure above.

2.2. Sampling Methods

Fish were caught with bottom and surface gill nets (100 m long × 3 m high, with a 20-mm mesh) and a seine net (15 m long × 2 m high, with a 12-mm mesh). The sampling effort was carried out to include potential differences in the bottom, water column, and depth using sampling tools that allow access to the entire water column. Samples were collected between October 2006 and May 2007, and one fish sample was collected by each tool in each month during daytime at weekly intervals in the three areas. A total of 288 fish samples were collected. Two replicates (bottom and surface gill net) were performed in the three areas, and each net covered an area of approximately 2000 m2, according to the following equation (see NEVES et al., 2010): A(area) = D × L, where D is the distance from the margin (100 m), and L is the net length effectively used in the haul (200 m). In shallow zones, fish were collected with a seine net, and the distance travelled was obtained using coordinates documented at the beginning and the end of each trawl with a global positioning system (GPS, Garmin III) to determine the swept area. For each sample (one for each weekly sampling in each area), the swept area (A) was estimated as follows: A = D × h × X2, where D is the length of the path, h is the length of the head rope, and X2 is the fraction of the head rope that encompasses the width of the path swept by the trawl (SPARRE and VENEMA, 1995). In this study, seine net samples were collected at speeds between 0.5 to 1 m/s, and it was assumed 2 that X2 = 0.3, with the swept area corresponding to approximately 210 m . All three fishing methods are directly related to the area sampled, and thus, fish densities were comparable. The catch per unit area was used to estimate density and was calculated by dividing the catch by the sampled area (individuals m–2 × 102). However, caution is needed when interpreting the results of these samplings, as noted by NEVES et al. 2010, because of possible influences of different techniques. WOLTER and BISCHOFF (2001) and LEEUW et al. (2007) also used different fishing methods to assess different habitats. Once captured, the fish were transferred to 10% formalin, and their total length (mm) and biomass (g) were measured in the laboratory. A Niskin water sampler was used to collect five surface and five bottom water samples on each sampling occasion (for each week and each month in the three areas), and to measure dissolved oxygen. A total of 960 samples were analyzed using a Digimed oximeter with a resolution of 0.01 mg/L

2.3. Statistical Analysis

Analyses of variance were performed to determine whether there were significant differences in fish abundance, biomass, length or number of species among the time periods evaluated, methods of capture and sampled areas. A three-way ANOVA was used to test for differences in the fish community parameters among the sampling months (October/2006 to May/2007), methods of capture surface net (SN), bottom net (BN) and seine net drag (SND) and sampled areas (1, 2 and 3). Pearson correlations were performed to verify whether there were significant correlations between abundance and richness with O2 (ZAR, 1999). The data were log10 (x + 1) transformed to address the assumptions of normality and homoscedasticity of the distribution. Cochran’s test was used to check the homogeneity of variances (UNDERWOOD, 2007). Tukey’s multiple comparisons test was used whenever significant differences were detected (DAY and QUINN, 1989). The alpha value was corrected by Bonferroni’s method (0.01) to avoid Type I Error (UNDERWOOD, 1981). Multidimensional scaling (MDS) was performed based on a matrix of 96 samples integrating the three collection methods for every week. This helped to evaluate potential differences in the fish assemblage at different times. This method is the most generally effective ordination method for ecological communities (MACCUNE and GRACE, 2002), and comparative studies have consistently demonstrated its reliability (CLARKE and AINSWORTH, 1993). An analysis of similarity (ANOSIM) was performed to evaluate the similarity between groups of samples corresponding to periods before, during and after the red tide. The abundance and biomass comparison (ABC) method was used to determine levels of disturbance of the estuarine fish fauna during temporal variations (CLARKE and WARWICK, 1994). The statistical package Primer 5 was used for all the above analyses.

3. Results

3.1. Dissolved oxygen

In the period before the red tide, the oxygen concentration varied between 6.7 (± 2.5) and 10.2 (± 2.3) mg/L–1 in the surface waters. Near the sediment, the concentration ranged between 5.7 (± 3) and 9.3 (±2.8) mg/L–1. During the red tide event, there was a clear reduction in the levels of O2 (Fig. 2). An anomalous condition was initially observed, with reduced oxygen levels being measured at the surface (below 2.0 mg/L–1), during the two first weeks of the red tide, and values of 2.8 to 4.3 mg/L–1 being recorded near the sediment. However, after the second week of the red tide, there was an increase of O2 in the surface samples and a decrease in bottom samples, which reached values below 3.0 mg/L–1. After the fourth week of the red tide event, by early April, there was a gradual return of O2 concentration values to levels similar to before the red tide. This suggests a tendency for normalization and indicates a trend of decreased variability for this variable.

Figure 2. Variation of dissolved oxygen in the study area during the red tide episode that occurred in Todos os Santos bay. Five samplings were performed per week at both the surface and bottom in three areas (1, 2 and 3; see Fig. 1). The samplings were always performed with the capture tools in place in the water between 06 : 00 and 12 : 00 h.

Figure 3. Dominant species in each study period: before, during and after the red tide. (Cet ede = Cetengraulis edentulus, Hae ste = Haemulon stendachneri, Euc arg = Eucinostomus argenteus, Sph gre = Sphoeroides greeleyi, Lut syn = Lutjanus synagris, Ath bra = Atherinella brasiliensis, Euc gul = Eucinostomus gula).

Figure 4. Mean number of individuals, biomass and length and the number of species in all samples collected in study periods: before, during and after the red tide.

3.2. Composition of fish fauna

From the 288 fish samples, a total of 1989 individuals, weighing 51.4 kg, belonging to 42 species in 29 families were captured with both net types. In the samples collected before the red tide period, the most abundant species were Cetengraulis edentulus, Haemulon stendachneri, Eucinostomus argenteus, Sphoeroides greeleyi, Lutjanus synagris, Atherinella brasiliensis and Eucinostomus gula (Fig. 3). The mean numbers of individuals, species and biomass were higher before than during or after the red tide (Fig. 4). During the period of the red tide, there was a dramatic change in the fish assemblage, and new species dominated the captures. Initially, pelagic and demersal species with high mobility, such as Cetengraulis edentulus, Anchoa januaria, Anchovia clupeoides, Centropomus undecimalis and Caranx latus, were severely affected, as they were not caught during the red tide event. The abundance and biomass of Sphoeroides greeleyi and Atherinella brasiliensis did not change during the red tide. Thus, they were the dominant species during the first two weeks (Fig. 2). After the dying out of the red tide, fish species that dominated before the event showed an increase in abundance and biomass (Fig. 3).

3.3. Temporal, spatial and methodological variations

During the red tide period, there were significant reductions in the abundance and number of species (p = 0.001 and 0.002, respectively) detected using the three sampling methods (Fig. 4). Table 1 shows the ANOVA results for each sampling month, sampling method and area. The surface gill net caught more fish than the bottom gill net before the period of the red tide (p = 0.009) owing to the possibility of sampling species that form shoals and swim closer to the surface. During the period of the red tide, the surface gill net method captured the least fish, both in terms of fewer individuals and species being collected (Fig. 4). The bottom gill net captured a lower number of individuals than the other two methods (p = 0.01), except during periods of a red tide event. The seine net was more effective

Table 1. Summary of the results of ANOVA for the number of individuals, species, length and biomass. Analysis performed on log10 (x + 1) transformed data. Differences among temporal variations, areas and periods determined by Tukey’s post-hoc comparisons; ns: not significant; MBR: months before red tide; DR: during red tide; MAR: months after red tide: SN: surface net; BN: bottom net; SND: seine net drag.

Source of variance

Temporal variation Areas Methods Interac- (1) (2) (3) tions

Nº of F = 16.75 p = 0.001 ns F = 10.33 p = 0,009 p = 0.001 individuals MBR > MAR > DR SN SND > BN 1 × 2 Nº of F = 15.05 p = 0.002 ns F = 13.19 p = 0.001 ns species MBR MAR > DR SND BN > SN Length ns ns F = 8.72 p = 0.01 ns BN SN > SND Biomass F = 14.35 p = 0.003 ns F = 13.98 p = 0.003 ns MBR MAR > DR BN SN > SND in collecting fish and captured the effect of the red tide on the fish assemblage, with a lower number of individuals being collected in March (p = 0.001) than in the other months (Table 1). The length of fish was different among the sampling methods (p = 0.01) (Fig. 4), with surface gill nets capturing larger individuals. However, in relation the red tide event, the difference was not significant. The lowest values for fish biomass were measured during the red tide (p = 0.003), and surface capture by the gill net was the least effective method of collection (p = 0.003) (Fig. 4). The temporal variation vs. sampling method interaction was significant (p = 0.001, see Table 1) for the number of individuals where the surface gill

Figure 5. MDS graph showing the study periods: three months before, during and two months after the red tide. black square = before, black triangle = during, and white square = after.

© 2012 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com 396 J. A. REIS-FILHO et al. net captured more fish before and after the red tide (p = 0.009). Positive and significant correlations between abundance (r = 0.89; p = 0.001) and richness (r = 0.69; p = 0.003) with O2 were also found.

3.4. Patterns in the fish fauna structure

The MDS ordination (Fig. 5) showed that the samples, collected in the periods before and after the red tide, were more similar than those taken during the red tide period. This was confirmed mainly by larger catches and more species. MDS showed that the samples collected during the red tide were ordinated in the second group (R = 0.62; p = 0.02) and were represented by the lowest values for abundance and number of species. The ABC plots for the fish fauna over time (Fig. 6) showed that, in most of the sampling months, the biomass curve exceeded the abundance curve in terms of cumulative dominance. This pattern is quite evident in the months that preceded the red tide (w > 0). In contrast, in March, when the red tide took place, the abundance curve exceeded the biomass curve (w < 0), although the original pattern was restored in the following months, when the biomass curve apparently returned to its previous condition.

Figure 6. Curves of cumulative dominance per rank species (ABC) for the sampled months based on data on abundance and biomass.

4. Discussion

4.1. Impacts of the red tide on the fish fauna

According to BLABER (2000), mass mortalities of fish are not uncommon in estuarine environments. In some cases, this can be the result of natural phenomena (e.g., typhoons, hurricanes), but other causes may reflect human activities (e.g., oil spills, industrial or urban wastes). The present study assessed the effect of a red tide (especially A. sanguinea) on estuarine fish assemblages on a local scale. In the past, the dinoflagellate observed in the present study, A. sanguinea, was assumed to be a non-toxic species. However, it is still considered to be harmful and it frequently predominates in red tides occurring throughout the world’s coastal waters (e.g., ROJAS DE MENDIOLA, 1979; ROBINSON and BROWN, 1983). Nevertheless, according to recent studies, it remains uncertain whether A. sanguinea can produce toxins (ZINGONE et al., 2006). Despite well-described reactions of avoidance in zooplankton populations (FIEDLER, 1982), the harmfulness of A. sanguinea is still unconfirmed, but it may have effects related to ich- thyotoxicity (ZINGONE et al., 2006). The high and unusual volume of freshwater inflow, in the headwaters of the Paraguaçu River, reflected heavy rains (Fig. 7), which contributed to an increase in the amounts of humic substances (HS) discharged into the bay. This in turn had a stimulatory effect of freshwater runoff on dinoflagellate production in coastal waters (PRAKASH and RASCHID, 1968). Large extensions of density-stabilized brackish water areas, associated with river plumes with enriched HS concentrations, tend to reduce the turbulence and shear generated by wind and currents through the formation of a density barrier (GAGNON et al., 2005). In addition to the occurrence of this phenomenon, which lowered salinity to values under 30 (BAHIA, 2007), the weather conditions in the preceding weeks

Figure 7. Paraguaçu River freshwater inflow into Todos os Santos Bay for February and March 2007 (Source: UHEPC).

© 2012 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com 398 J. A. REIS-FILHO et al. of mid-summer were very stable. Low wind intensity and no rain, were also atypical. A similar situation was documented by KAHRU and MITCHELL (2004) in Paracas Bay (Peru) in the summer of 2004 following a large input of freshwater from the adjacent Pisco River. Indeed, GAGNON et al. (2005) provided evidence for the stimulatory potential of HS on the growth of a dinoflagellate (Alexandrium tamarense) and pointed out that increased freshwater and reduced turbulence favor the growth of dinoflagellates in the St. Lawrence Estuary (Canada). This supports the findings of other authors. Under experimental conditions, the addition of HS extracts was found to significantly increase the growth rate of A. tamarense, even at the lowest concentrations tested. This suggests that this dinoflagellate probably shared a common growth-stimulating mechanism. DOUCETTE and HARRISON (1990) pointed out that iron limitation could represent a limiting factor for A. sanguinea and therefore be an important issue in red tide ecology. In this context, in the presence of high hydrogen sulfide concentrations, iron availability may prevail, limiting the iron limitation pattern. Although A. sanguinea is not known to produce toxins, blooms of this species have coincided with fish, crustacean and oyster mortality in many places (BRICELJ et al., 1992; ROBICHAUX et al., 1998; WU et al., 2000). Such mortality may be due to clogging of shellfish and fish gills, to oxygen depletion following the blooms (WARDLE et al., 1998; HORNER, 2002; GRANÉLI and TURNER, 2008), or to a powerful surfactant than can act a lytic agent on gills (JESSUP et al., 2009). Fish necropsy indicated that the gills of most of the examined fish were clogged (ALBINATTI, pers. com.), and that their digestive parts were full of food. This suggests that the animals were in a better condition previously, and that death occurred under acute circumstances (Projeto Mamíferos Marinhos, unpublished data). In the present study the reduction of dissolved oxygen, corresponding to the red tide period, could be associated with a depletion of fish abundance and richness. The effects of a red tide can be more intense on planktivorous fish (SUBRAMANIAN et al., 1994), probably because plankton are affected quickly owing to the excessive proliferation of a few species. In the present study, Cetengraulis edentulus, a pelagic fish species that forms large shoals and was dominant prior to the occurrence of the red tide, was the most affected species. It has been suggested that fish from this family are the major contributors to the flux of energy along the estuarine food chain, especially where they are the largest zooplankton consumers (BAIRD and ULANOWICZ, 1989). Our data support evidence that fish mortality occurred due to gills clogging from a high algal density, especially for C. edentulus, but the synergistic effect of low oxygen concentrations cannot be ruled out as low O2 concentrations were detected during the red tide. ABC curves assume that in a stable environment, large-sized individuals are present and, although they represent a small portion of the total abundance, they play a predominant role in terms of biomass (WARWICK, 1986). When the curves of the dominance of abundance and richness per rank species are plotted, the biomass curve seems to exceed the abundance. In the presence of disturbances in the environment, species that require better environmental conditions are at a disadvantage, and small-sized opportunist species may also become dominant in terms of biomass. With numerical dominance of small-sized species, an inversion of the curves may occur, with the biomass curve being exceeded by the abundance curve. In the first two weeks of the red tide event, when mass mortality was apparent, Sphoeroides greeleyi occurred in large groups in the intertidal zone. FAVARO et al. (2009) reported this species as being common in intertidal environments and it is considered important for the trophic balance in coastal environments (DUNCAN and SZELISTOWSKI, 1998; SCHULTZ et al., 2002). Atherinella brasiliensis is a typical species that forms shoals in shallow estuarine regions (BARBIERI et al., 1991; ANDREATA et al., 1997, 1997; HOSTIM-SILVA et al., 1995; PESSANHA et al., 2000; RAMOS and VIEIRA, 2001). These two species were the most abundant during the red tide. S. greeleyi, which was the fourth most captured species before the red tide, reached the first position during the event, although with a lower abundance than previously. Thus suggesting a resistance to the red tide.

FAVARO et al. (2009) found that the largest catches of S. greeleyi occurred between the end of spring and beginning of autumn. This period coincided with the occurrence of speci- mens of smaller size and with a lower mean body mass. The present study was conducted from the end of spring until the beginning of autumn, and most of the individuals of this species exhibited a size corresponding to adult fish. Thus, it appears that the increase in catches of this species, in the period of the red tide, might not have been due to the numbers of juveniles present. However, A. brasiliensis, which was not among the most abundant fish before the red tide period, emerged as dominant during the red tide event. This took place with even lower abundance in relation to the dominant species before the red tide. This species has previously been recorded in large numbers in areas under environmental stress caused by anthropogenic activity near the Paranaguá Port in Southern Brazil (FALCÃO, 2005). Consequently, when there are disturbances, conservative species are at a disadvantage, and small-sized opportunist species become dominant. Numerical dominance of small-sized species was the cause of the inversion of the ABC curves, as the biomass was exceeded by abundance during the red tide period in the region. In the Chesapeake Bay (USA), Jung (2001) showed, that the ratio of abundance to biomass was directly related to the occurrence of juvenile fish in shallow areas. OTERO et al. (2006) showed that sampling methods (fishing gear) may influence this relationship, and suggested that such factors determine the ratio of abundance to biomass. In the present study, the different sampling methods and different depth zones evaluated coincide with the above author’s concerns, as most of Todos os Santos Bay is dominated by ebb-tidal deltas during low tide conditions (LESSA et al., 2001). Soon after the red tide event, we noted that there was a return of the values for abundance, number of species and O2, and a return of dominant fish species to conditions prior to the red tide. Recent studies have indicated that fish populations often exhibit a non-linear nature and have the potential to shift dramatically in a short period of time (HSIEH et al., 2010). Their recovery trajectories have been described related to coral assemblages after impacts such as natural disasters (e.g., cyclone and bleaching events) (ADJEROUD et al., 2009). However, in addition to fishery exploitation, environmental variations (e.g., red tides) play important roles in affecting fish populations (BOTSFORD et al., 1997). They alter spatial structures and cause affected fish to be more prone to catastrophic shifts (HSIEH et al., 2010). Fluctuations of fish communities can clearly be affected by both environmental forcing and fish mortality (JACKSON et al., 2001; MCFARLANE et al., 2002). If a fish species exhibits several populations living in separate locations, each of which is characterized by distinct ecological parameters (e.g., specific habit and tolerance to environmental variations) (HSIEH et al., 2010), then some populations may encounter habitat failure (due to environmental stochasticity), and other populations may succeed. This may reflect the “rescue effect” (RICKLEFS, 2003), where there is immigration of large and productive subpopulations, which in turn decrease subpopulations to the point of extreme values. Fol- lowing high mortalities, due to hypoxia in shallow waters of Coliumo Bay (Chile), a rapid recovery of the fish community was also observed (HERNÀNDEZ-MIRANDA et al., 2010). It is possible that the recovery of oxygen has contributed to the return of the fish community affected by the red tide. Furthermore, the high productivity of the intertidal environment ensures rapid recovery of the levels of dissolved nutrients and favors the support of many aquatic organisms (UEDA et al., 2000). This effect of restoration (rescue effect), which can be incorporated into metapopulation models and has been widely recognized in terrestrial systems, has been largely ignored in aquatic systems. This reflects the fact that there is no clear barrier in the ocean and that larval dispersal is common for many fish and invertebrate species (MCQUINN, 1997; KRITZER and SALE, 2004). Perhaps this concept may be applied to marine regions with tangible geographic limits in bays and estuaries.

In Todos os Santos Bay, more than one million people are employed in fishing, agriculture and industrial activities (LESSA et al., 2001). Some human activities result in adverse effects due to introduced contaminants and nutrients (HATJE and ANDRADE, 2009). Additionally, the rapid increase in the input of plant nutrients, particularly nitrogen compounds, into coastal waters throughout the world reflects the growing disposal of sewage from expanding populations, increased use of chemical fertilizers in agriculture and increased fossil fuel combustion (SMAYDA, 1989; ANDERSON et al., 2002). Thus, increasing linkages between nutrient loading and estuarine/coastal marine HAB have recently been recognized (SMAYDA, 1990, 1997; ANDERSON et al., 2002; GLIBERT et al., 2005). The relationship between alterations in the nutrient composition and the development of HAB is supported by examples from freshwa- ters, estuaries and marine coastal waters worldwide (reviewed by ANDERSON et al., 2002). HEISLER et al. (2008) provided consistent information on the role of nutrient enrichment in estuarine and marine HAB. Indeed, this condition applies to TBS; however, during the phenomenon addressed in the present study, a combination of factors (nutrient enrichment, climatic stability and a high fresh water input) appears to have played an effective role in HAB formation.

5. Conclusions

In spite of the non-systematic effort of environmental authorities to assess the causes of fish mortality, a A. sanguinea bloom did occur, as indicated by water color and a high cell density. A combination of factors, including climate stability (few winds, no rain, high tem- perature) associated with an abnormally HS-rich water flow, probably provided ideal conditions to trigger the dinoflagellate bloom. The absence of such blooms in subsequent years may also help confirm this. Still, the ichthyofauna of the studied areas, where the red tides occurred, responded with changes in the community and highlighted some resistant species. The importance of different strains in HAB, as pointed out by WOOD and LEATHAM (1992), cannot be ignored, and this factor may represent a difficult task in coastal environmental management. The present study showed that the dynamics of small populations of fish are often influenced by fortuitous events, such that stochasticity or random events may influence community dynamics. We have gathered reliable information to corroborate the fact that the fish community did undergo changes owing to the algal bloom. This study provides analysis on a small scale, with some degree of refinement of structural changes in the fish assemblage, which may shed light on some points that remain unclear regarding the fish mass mortality attributed to red tides.

6. Acknowledgements

We thank H. JOHNSON (EUA) and A. F. DA SILVA (Universidade Federal Fluminense) for improving the English manuscript. The Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) provided a scholarship to J. A. REIS-FILHO. The Catholic University of Salvador and the Federal Uni- versity of Bahia provided the infra-structure and facilites for the work. F. BARROS, J. A. C. C NUNES and E. M. DA SILVA acknowledge receiving CNPq fellowships.

7. References

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Manuscript submitted September 5th, 2011; revised November 30th, 2011; accepted: December 6th, 2011