Community structure of the ichthyofauna associated with seagrass beds ( Halodule wrightii ) in Formoso River estuary – Pernambuco , Brazil

Seagrass beds are used by juvenile fishes in different ways, generally as nursery sites, shelter from predators, reducing competition and increasing availability of food resources, thus establishing a relationship of connectivity with other ecosystems. In the present study, the community structure of the ichthyofauna associated with seagrass beds on the Formoso River (Pernambuco – Brazil) was evaluated during the winter of 2008. Twenty-seven manual trawls (15 daytime and 12 nighttime) were performed, and a total of 358 fishes belonging to 18 families, 21 genus and 25 species were collected. The Catch Per Unit Effort (CPUE) by trawling average was 13.5 and 4.95 individuals per species per trawl. The most abundant families were Scaridae (n = 111), Tetraodontidae (n = 63), Lutjanidae (n = 56), Mullidae (n = 39) and Engraulidae (n = 19). Ecological indices for dial changes were always higher for the night period, confirming that such areas are used more frequently during this period. The need for measures to conserve these areas is emphasized, by its importance and vulnerability to human impacts.


INTRODUCTION
The use of seagrass beds by several species of fishes has received considerable attention because of the connection between, the mangroves and coral reefs (Pollard 1984, Parrish 1989, Beck et al. 2001).However, the importance of these ecosystems for reefs/estuarines fishes has not been adequately quantified.It is necessary to know the real function of seagrass beds as refuge areas from predators, areas of decreased competition and increased availability of food resources (Blaber and Blaber 1980, Laegdsgaard and Johnson 2001, Adams and Ebersole 2002).
The protection and management of seagrass beds environments are essential for the survival of many marine species connected to coral reefs, sand plains and estuaries, forming a mosaic of shallow water environ-ments (Beck et al. 2001).Important ecological connections among these ecosystems include energy flow and use of a combination of habitats throughout the life cycle of animals, determined by ontogenetic migration (Meyer et al. 1983, Parrish 1989).
Non-reef habitats located near the reef systems act as buffer areas.They keep the recruitment levels even during the periods in which they are low, and act as corridors ("stepping stones") where fishes move freely while keeping the connectivity among the habits of juvenile, subadult and adults (Laegdsgaard and Johnson 1995, Gillanders et al. 2003, Mumby et al. 2003).
Many families of reef fishes with ecological and economic importance (e.g.Haemulidae, Lutjanidae, Mullidae and Scaridae) migrate among the areas that maintain connectivity among coastal ecosystems (Beck et al. 2001).Large aggregations of juveniles of Haemulidae, for example, are found close to areas of man-groves, seagrass and coral reefs and, thus, perform ontogenetic migrations among these areas, which involve changes in diet and behavior (Lindeman et al. 2000, Cocheret de la Morinière et al. 2003).
Several studies have been performed worldwide describing the community of the ichthyofauna in seagrass areas (e.g.Weinstein and Heck 1979, Verweij et al. 2006, Allen et al. 2007, Lugendo et al. 2007, Nakamura and Tsuchiya 2008).In Brazil, few studies have been conducted (Schwamborn 2004, Rezende 2008), and there is a clear need for extending this line of studies to improve the understanding of ecological relationships in these ecosystems.
This study aims to evaluate the community structure of the ichthyofauna associated with seagrass beds of Formoso River estuary during the winter months (June to August) in Tamandaré municipality, Pernambuco State.Species composition, abundance, diversity, size/weight data and trophic guilds were used to describe the fish community.

STUDY AREA
The study area is included in the limits of two multipleuse protected areas: "APA de Guadalupe" and "APA Costa dos Corais".
The Environmental Protection Area (EPA) de Guadalupe is spread to continental and marine areas and covers four municipalities: Sirinhaém, Formoso River, Tamandaré and Barreiros.The Environmental Protection Area (APA) Costa dos Corais, extended to over 135 km of coastline from Tamandaré, southern state of Pernambuco, to Maceió, state of Alagoas, and is the first unit of the federal conservation that includes coastal reefs.It is also the largest marine conservation unit in Brazil (Ferreira and Cava 2001).
The study was conducted in the municipality of Tamandaré (Fig. 1), which is characterized by reef formations parallel to the coast.It has a tropical climate with a dry season from October to March, with temperatures around 30 The seagrass beds found in the area are mainly composed by Halodule wrightii, which are positioned parallel to the coastline and are spread over a small part of Carneiros beach.They are usually inserted among plains of sand, with an average depth between 0.5 and 2.0 m and making patches of short extensions.Channels are reported between the sand plans and the seagrass meadows, which can be used for the migration of species in general (personal observation).SAMPLING Samples were collected monthly during day and nightime in the seagrass beds in the winter months (June to August) using a manually operated bottom trawl for capturing juvenile fishes and settlers.It consisted of a PVC frame 1,5 × 1,0 m, with a 5 mm mesh.Trawling was performed parallel to the coast-line and at random location for three minutes each.No nocturnal sampling was held during the month of June due to logistical conditions.
After the completion of trawls, all the collected material was sorted.Fishes were separated and placed in a plastic tray with sea water while the remaining material (invertebrates, algae and sediment) were promptly returned to the ocean.The collected fishes were taken to the laboratory of CEPENE/IBAMA, and individuals were weighed, measured and included in classes of length, then fixed in a solution of 10% formalin and preserved in alcohol 70 • GL.The Catch Per Unit Effort (CPUE) was calculated for each trawl and was (Ind./Trawl)= Number of individuals per trawl.
At all the sampling points the temperature ( • C) and surface water salinity (PSU) were measured.

DATA ANALYSIS
Indices were calculated to compare the ichthyofauna between day periods and months of samples.The diversity index of Shannon-Wiener (H'), species richness of Margalef (D) and equitability of Pielou (J') were calculated using the software Species Diversity Richness, version 1.2.
To compare the number of species that occurred during the day and night time, a G test (Zar 1999 logical indices, the Kruskal-Wallis test (Zar 1999) was used, both available on BioEstat 3.1 software (Ayres et al. 2003).Normality and homogeneity of variances were tested using the software StatView (Roth et al. 1995).

RESULTS
Twenty-seven manual trawls (15 daytime and 12 nocturnal) were performed during winter months (June to August 2008).A total of 358 individuals were collected, weighed, measured and identified to the species level, corresponding to 18 families, 21 genera and 25 species.The average catch was of 13.5 individuals per trawl, with a maximum of 35 individuals and a minimum of three, while the average species richness was of 4.95 species per trawl, with a maximum of 10 species and a minimum of one (Table I).
Environmental conditions in winter were of lower temperatures and higher pluviosity in the region.The minimum temperature recorded was 24.5 • C and maximum of 26.5 • C, whereas the minimum recorded salinity was 32.1 PSU and the maximum was 38.3 PSU.
The analysis of abundance by CPUE (Ind./Trawl),considering the more representative five families, indicated the family Scaridae as the most abundant (average of 4.11 Ind./Trawl) (Fig. 2).

DIEL VARIATION IN THE ABUNDANCE
AND COMPOSITION OF THE ICHTHYOFAUNA A total of five species were collected only in daytime samples: Bodianus rufus, Dactylopterus volitans, Doratonotus megalepis, Mycteroperca bonaci and Rypticus saponaceus which represent 18.5% of total collected taxa.Besides, these eight species were collected only during nighttime: Anchoa sp., Barbulifer ceuthoecus, Eucinostomus lefroyi, Hemiramphus brasiliensis, Mulloidichthys martinicus, Sparisoma frondosum, Sphoeroides greeleyi and Stephanolepis hispidus, which represents 29.6% of the total collected, thus, showing the highest species richness at night.Fourteen taxa were collected during the day and at night, representing 51.8% of the total.
A significant difference among the species collected during the daytime and at night was found (G = 130.51, df = 24, p<0.01), showing the use of the area by different species of the community at different periods of the day.

LENGTH AND WEIGHT COMPOSITION
The lowest total length (TL) observed was 1.0 cm for a Sphoeroides testudineus specimen, and the largest collected individual was a specimen of Hemiramphus brasiliensis with 20.0 cm of total length.The species that showed the larger range of length was Scorpaena plumieri -average of 14.2 cm, ranging from 4.0 to 18.2 cm, and the smaller was Sphoeroides greeleyi -average of 0.3 cm, ranging from 1.5 to 1.8 cm (Table III).
Regarding weight patterns, the highest value was recorded for the species Scorpaena plumieri -155.10 g, and the lowest (0.10 g) for several species: Syngnathus folletti, Lutjanus synagris, Sparisoma axillare, Ctenogobius saepepallens, and Sphoeroides spengleri.The species that showed the greater weight range was Scorpaena plumieri -average of 153.30 g, ranging from 1.80 to 155.10, and the smaller was Syngnathus folletti -0.10 g, ranging from 0.10 to 0.20 g (Table III).
For most of species (72.0%; n = 18), the average TL is lower than the 10% of maximum total length found in the literature.Thus, individuals can be considered recruits or juveniles.

DIVERSITY, RICHNESS AND EQUITABILITY
OF THE ICHTHYOFAUNA For the total fish community, the ecological indices values were: Shannon-Wiener diversity (H' = 2.66, standard deviation = 0.0042), Richness of Margalef (D = 4.15) and Pielou equitability (J' = 0705).The obtained values per month and per period (daytime and nighttime) are given in Figure 4.
There was no significant differences among the analyzed months (Fig. 4A) (H = 0462, df = 2, p>0.05), indicating a small fluctuation in the community over the winter months.

DISCUSSION
It is well known that the density of fishes associated with marine seagrass beds is directly related to leaf area of plant and structural complexity of the dominant algae (Jernakoff et al. 1996).The studied area is characterized by the predominance of the species Halodule wrightii, which is among the species of smaller leaf surface (Jernakoff et al. 1996).
Ichthyofauna studies in mangroves areas and seagrass beds showed that such sites have a relatively high number of species (Nagelkerken et al. 2000, Unsworth et al. 2007).However, a small number of species dominates the structure of the local community in terms of numerical abundance (Quinn 1980, Lugendo et al. 2007).In Madagascar, for example, five species were found representing this total (Laroche et al. 1997); in Australia, only three species (Kwak and Klumpp 2004) were found and in an estuary in the Northeast Brazil (Barletta et al. 2005), six species.In the present study, by analyzing just the winter months (June, July and August), this trend was confirmed, with eight species representing 81% of the whole community sampled.
The understanding of changes in the abundance and diversity of fish fauna in seagrass meadows during day/night periods is a key factor to understand the community dynamics (Bell and Harmelin-Vivien 1982, Cocheret de la Morinière et al. 2003, Lugendo et al. 2007).Many previous studies concluded that both the number and density of species were higher at night (Baelde 1990, Nagelkerken et al. 2000, Letourneur et al. 2001, Jelbart et al. 2007), mainly due to the fact that many species use the reef environment as a structural refuge during the day, but depending on the seagrass beds and other areas of connectivity to feed at night and dusk.This same pattern was confirmed in this study with values always higher at night.
Studies of faunal communities in seagrass meadows on the coast of Pernambuco were conducted by Ramos (1973), M.S. Alves (unpublished data), G.F.S. Viana (unpublished data), Alves (2000), Schwamborn (2004) and Rezende ( 2008), four of them emphasizing fish commu-An Acad Bras Cienc (2010) 82 (3)  nities.The equipment and methodology used in this study is similar to those used in Schwamborn (2004) and Rezende (2008); however, it was performed manually and only during the winter (rainy season).This maneuver brought some advantages, as the noise of the motorboat engine may drive off individuals and, thus, increase the selectivity of larger size fishes, with more ability to swim.Therefore, the sampling method used in the present study is probably more robust in this respect.
For the seagrass beds of Itamaracá -Pernambuco State, Schwamborn (2004) found that the Shannon-Wiener index (H' = 1.43) and the richness index of Margalef (D = 3.00 to 4.4) showed the highest values during the rainy season.The values reported in the present study were higher than those observed by Schwamborn (2004).
Analyzing the ichthyofauna in the same site of this study, Rezende (2008) found the highest values of diversity and equitability in the warmer months (dry sea-An Acad Bras Cienc (2010) 82 (3) son).In June, Rezende ( 2008) obtained (H' = 1.52 and J' = 0.38), and this study (H' = 1.75 and J' = 0.54); in July, (H' = 1.66 and J' = 0.41), and this study (H' = 2.23 and J' = 0.69); and in August, (H' = 1.47 and J' = 0.36), and this study (H' = 1.73 and J' = 0.53).It was noted that the values of diversity were very similar.However in the present study, they were higher, possibly due to the aforementioned methodological problems using motorboat.
Comparing the species composition with a survey of reefs in the region of Tamandaré (Ferreira and Cava 2001), 20 species (80.0%) were also found in the reef environments.When the same comparison is made with the estuarine ichthyofauna obtained during a study in the same region (F.L.B.Santos, unpublished data), only nine (36.3%) and (Paiva et al. 2008) ten species (40.0%) that occurred in the estuary of the Formoso River were collected in the meadow.Therefore, we suggest that the species composition of seagrass beds has a greater influence of reef environments.
The mobile invertebrate feeders trophic guild was the most representative.This fact was also evidenced in several seagrass beds throughout the world (Greenway 1995, Nakamura et al. 2003, Allen et al. 2006, Unsworth et al. 2007).The preference for these environments by the ichthyofauna is due to the large availability of invertebrates (crustaceans, polychaets and molluscs) living in association with the seagrass (Nakamura andSano 2005, Casares andCreed 2008).
The presence in this seagrass of a large number of herbivores contradicts the theories related to feeding habits of herbivorous and seagrass beds (Bell andPollard 1989, Allen et al. 2006), where the abundance of herbivores and the consumption of algae by the community is low, despite the availability of the algae forming the meadows.However, another hypothesis, which corroborates the present study, argues that large herbivores use algae as a food resource (Lobel and Ogden 1981, Nakamura et al. 2003), specifically for individuals of the families Scaridae and Acanthuridae (Randall 1965, Ferreira andGonçalves 2006).
Marine seagrass beds worldwide are suffering a reduction of their areas due to the process of urbanization and human interference on the coast (Duarte 2002, Marques andCreed 2008).In several places, partial or even total degradation is found (Hemminga and Duarte 2000).This fact directly affects the fauna associated with this environment (Hovel and Lipcius 2001).According to the Global monitoring and information network for seagrass meadows -SeagrassNet (Short et al. 2006), a decline was observed in two populations in the Brazilian coast: one in Paraná State and the other in Abrolhos bank, Bahia State.The analyzed region in this study is within the limits of two marine protected areas, which enhances the need for management strategies of sustainable use and ecosystem conservation.Such strategies should include measures to protect the seagrass beds from a diversity of impacts, including the removal of algae.User restrictions to avoid trampling and tourism by avoiding the presence of vessels, for instance, is urgently needed, since these are important nursery sites for reef fishes.Fishery in reef environments is an activity of great social and economic importance in the region (Ferreira and Maida 2001), whose sustainability depends on the integrity of habitats that are essential to the fish fauna.

RESUMO
Fig. 1 -Map of the study area with the associated ecosystems (sand banks, seagrass beds and coral reefs).

Fig. 5 -
Fig. 5 -Trophic organization of the collected ichthyofauna for species and individuals during the winter on Carneiros beach, Tamandaré -PE.
• C and a rainy season between April and September, with temperatures around 26 • C (Maida and Ferreira 1997).Samples were collected at Carneiros beach (8 • 41 33 S and 35 • 05 14 W), which has a very diverse range of ecosystems (mangroves, sand banks, seagrass beds and coral reefs).