Decapod crustaceans from a marine tropical mangrove ecosystem on the Southern Western Atlantic , Brazil

The purpose of the present study was to investigate the biodiversity, relative abundance and frequency of decapod crustaceans in the marine mangrove ecosystem at Gaibu Beach, Pernambuco State, Brazil. A total of eight samples were taken: four in the rainy season (August 2010) and four in the dry season (February 2011), during spring low tides and according to the phases of the moon. In all, 352 decapods were sampled. These specimens belonged to 17 species, 14 genera and 13 families. Pachygrapsus transversus (Gibbes, 1850), P. gracilis (Saussure, 1858), Panopeus americanus Saussure, 1857 and Uca (Leptuca) leptodactyla Rathbun, 1898 were very frequent. The three latter species occurred in all samples. The most abundant species was P. americanus. The Shannon-Wiener index (H’) showed that, in general, the diversity level was medium for all samples. However, the sample taken at the time of the new moon during the rainy season was classified as highly diverse. These results contribute to the knowledge of the decapod fauna inhabiting mangroves associated with fringe reefs.


Introduction
The mangrove forest is a coastal ecosystem belonging to the transition zone between the land and the sea.It reflects strong tidal influence and is typical of tropical and subtropical regions (Schaeffer-Novelli, 1995).The mangrove ecosystem is considered one of the areas of the world with relatively high fertility, can provide valuable information about the dynamics of the littoral environment (Lacerda et al., 2006), and is one of the most important coastal ecosystems.This high fertility results from the influence of many factors, including the abundance of primary producers, tidal action, high nutrient input, of mangroves occurring in association with a fringe reef.This site is an enclave protected by sandy reefs on the seashore, with Laguncularia racemosa C. F. Gaertn occurring as a dominant species.The area is under the influence of the Arrombado Stream (Rolim et al., 2002).
According to Aveline (1980), the invertebrate fauna of mangrove forests is composed primarily of decapod crustacean species.These organisms play a significant role in the dynamics of the mangroves.In addition to their role as important participants in the trophic web, certain crustaceans constantly excavate burrows in the mud to obtain shelter and to store food.By digging in the sediment, they transport organic matter from the underlying strata to the surface (Araújo and Maciel, 1977;Macintosh, 1988).The crustaceans also participate in the cycling of nutrients, controlling the remineralization of detritus in the forest (Robertson, 1991).The purpose of the present study was to investigate the biodiversity of decapod crustaceans inhabiting the marine mangrove at Gaibu Beach and to compare these findings with those of other studies in marine and estuarine areas.

Study area
Gaibu Beach (Fig. 1) is located in the Municipality of Cabo de Santo Agostinho, southern Pernambuco, Brazil (8 º 19' S and 34 º 56' W).According to the Köppen (1936) classification, the climate type is As', i.e., a tropical humid climate with rainy winters and dry summers.The annual mean temperature is 25ºC.The beach can be considered intermediate in structure, showing an area of open sea and another area, larger and protected by two fringe reefs, in the infralittoral and intertidal.The mangrove is located in front of the intertidal fringe (CPRH, 1999).

Field procedures
Samples were taken during the spring low tide.Four samples were taken during the rainy season (August 2010) and four during the dry season (February 2011).The four samples during a given season were taken during different phases of the moon.As a result, a total of eight samples were performed: rainy period new moon (RPNM), rainy period waxing moon (RPWXM), rainy period full moon (RPFM), rainy period waning moon (RPWNM), dry period new moon (DPNM), dry period waxing moon (DPWXM), dry period full moon (DPFM) and dry period waning moon (DPWNM).
The individuals were randomly sampled by two collectors in the substratum (with a garden shovel), under rocks, in trees and in the water (with a dipnet), including every microhabitat within the mangrove.The specimens were fixed in 70% alcohol.The abiotic data collected during the sampling included air and water temperatures, measured in situ with a digital thermometer, and salinity and pH, determined from measurements of water samples in the laboratory.

Laboratory procedures
The pH was determined with a bench pH meter.The salinity was determined with the Mohr-Knudsen method (Strickland and Parsons, 1972).

Statistical analyses
The Student t test was applied to analyze the significance of the differences (α = 0.05) in each abiotic factor between the dry and rainy periods (Zar, 1999).The relative abundance (RA) of each species was obtained from the equation RA = n100/N (where n = the number of individuals of that species and N = the total number of individuals) and classified as dominant (≥ 70%), abundant (40 to 70%), less abundant (10 to 40%) and rare (≤ 10%).
The frequency of occurrence (FO) of each species was obtained from the equation FO = a100/A (where a = number of samples containing the species and A = the total number of samples), with a posterior classification as very frequent (≥ 70%), frequent (40 to 70%), less frequent (10 to 40%) and sporadic (≤ 10%).
Both temperatures were higher during the dry period.
A total of 352 decapods was sampled, including 17 species, 14 genera and 13 families.
The group with the highest number of species was the Infraorder Brachyura Linnaeus, 1758, with 10 species, followed by the Infraorder Anomura MacLeay, 1838 and Infraorder Caridea Dana, 1852b (3 species each) and the Infraorder Axiidea Huxley, 1879 (1 species) (Tab.1).Pachygrapsus transversus (Gibbes, 1850), P. gracilis (Saussure, 1858), Panopeus americanus Saussure, 1857 and Uca (Leptuca) leptodactyla Rathbun, 1898 occurred very frequently, especially the three latter species, which were recorded in all samples (Tab.2).According to the Shannon-Wiener index (H'), the diversity was medium for all samples except for the RPNM sample, which was classified as high in diversity.The values of the Pielou index (J') were greater than 0.5 and equitable in all samples.The Margalef index (d) was lower for the RPWNM (2.17) and higher for the RPNM (3.65), indicating a medium-diversity area (Tab.3).

Discussion
The water and air temperatures varied significantly between periods but showed only small oscillations among the samples.In the mangroves at Itamaracá Island, Pernambuco,  the temperatures similarly showed no substantial variation (Macedo et al., 1973;Araújo et al., 2012), a characteristic typical of tropical regions.At Enseada dos Corais Beach, located near the study area, the salinity was found to range between 9 and 36 (Florêncio, 2000), whereas the salinity at the mangrove of Gaibu Beach varied between 16.15 and 32.62, indicating a more saline and stable system.The samples obtained during the dry season showed a large decrease in salinity.According to SINDA ( 2012), an intense rainfall occurred on the day prior to this sample.The pH values were always alkaline, as previously observed by Araújo et al. (2012).
Several authors have previously investigated the diversity of decapods in estuarine mangroves.The species richness found at Gaibu Beach was lower than the richness previously found for these other localities (Tab.4).This lower diversity may be linked to the location of this study in a non-estuarine area.This location could be unsuitable for many species typical of estuarine mangroves, as Ucides cordatus (Linnaeus, 1763), Sesarma rectum Randall, 1840 and Goniopsis cruentata (Latreille, 1803), adapted to the variations occurring in the estuarine environment, including salinity, turbidity, and the type of substrate.Note that each locality can present their peculiar microhabitats and the sampling efforts in each study may have been different, which may also account for the different diversity among estuaries.
The Ocypodidae Rafinesque, 1815 and Grapsidae MacLeay, 1838 are usually the most diverse decapod crustacean families in mangrove ecosystems (Coelho, 1966;Jones, 1984;Macintosh, 1988;von Prahl et al., 1990;Cobo et al., 1994;Oshiro et al., 1998;Hartnoll et al., 2002;Echeverría-Sáenz et al., 2003).In the present study, the Ocypodidae were represented by a single species, Uca (L.) leptodactyla.Despite the annual oscillation in the temperature, this species was frequent and present in all samples.This finding shows that temperature is not a limiting factor for this eurythermic species.Similarly, Masunari (2006) observed this species in an area with a relatively broad range of temperature (13 to 35ºC).In addition, U. (L.) leptodactyla prefers high salinities (Crane, 1975;Barnwell, 1986;Thurman, 1998) and muddy sand substrata (Colpo and Negreiros-Fransozo, 2003;Benetti and Negreiros-Fransozo, 2004;Castiglioni and Negreiros-Fransozo, 2004), as observed in the present study, showing that the studied marine mangrove location has ideal characteristics as a habitat for this species.The family Grapsidae was represented by two very frequent but non-abundant species, Pachygrapsus transversus and P. gracilis.These species were rare and less abundant, respectively.Note that this mangrove forest is protected by a fringe reef and that this reef may provide a refuge for species that are difficult to sample, including those belonging to the genus Pachygrapsus Randall, 1840.For this reason, a more speciesspecific capture method should be applied to sample these crabs, as observed by Flores et al. (1998).
Panopeus americanus has normally been found in association with sandy-mud substrata (Masunari and Dubiaski-Silva, 1998), under stones, on muddy beaches and in mangroves (Melo, 1996), exactly the same habitats in which this species was found in this study.The finding that P. americanus was more abundant than the other species in the sample could be associated with the slow mobility of this species, which facilitated its capture.
In the samples, all the specimens of Callinectes exasperatus and C. marginatus (A.Milne-Edwards, 1861) (both members of the family Portunidae) were juveniles.For this reason, the marine mangrove ecosystem investigated in this study can be considered a nursery area for both species.Several papers have reported that juvenile Callinectes Stimpson, 1860 migrate to estuaries, where they find food and shelter from predation (Hines et al., 1987;Guerin and Stickle, 1997;Araújo et al., 2012).Although the Gaibu mangrove forest is not estuarine, it is protected by reefs.According to Melo (1996), C. exasperatus inhabits shallow waters from the intertidal to a depth of 8 m in the sea and in estuarine waters, near river mouths and in mangroves.Callinectes marginatus inhabits sandy and muddy bottoms, the periphery of mangroves, brackish water, and, rarely, open sea, from the intertidal to a depth of 25 m.Due to these ecological preferences, the Gaibu mangrove forest is a suitable habitat for the development of the juveniles.
The value of H' during the RPNM was the only one similar to that previously observed in the mangroves of the Caribbean (H' log 2 = 3.525) (J'= 0.869) and of the Pacific coasts of Panama (H' log 2 = 3.704) (J'= 0.857) (Abele, 1974), whereas the other samples of the present study showed lower values.During the rainy period, phytoplankton production is less intense (Passavante and Feitosa, 2004).This decrease in production could result in a decrease in the availability of food to the decapods and could thus reduce their abundance.However, the days are significantly shorter during the winter in the temperate zones (Brosche and Sündermann, 1990), and slightly shorter in tropical ones.This difference associated with the absence of light on new moon nights, reduces the risk of predation.For this reason, this community may be affected more strongly by the action of predators (top-down control) than by the amount of food available (bottomup control) (Uye and Liang, 1998).The results presented in this paper contribute to the knowledge of the decapod fauna inhabiting mangroves associated with fringe reefs, a rare and poorly studied habitat.Bezerra (UFERSA) and Dr. Alexandre Oliveira de Almeida (UESC) for aid in the identification of the animals.The first author thanks the Universidade Federal de Pernambuco (UFPE) for a scholarship granted by the Program of Academic Maintenance.The second author thanks the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for a doctoral scholarship.We also thank our past supervisor and friend Dr. Petrônio Alves Coelho, in memoriam, for all his support and encouragement of our work on this study.From the inception of this undergraduate project to the analyses of the data, he was always available to help us.The authors are thankful for the suggestions offered by the anonymous referees on the first version of the manuscript and by the American Journal Experts for the English editing.

Figure 1 .
Figure 1.Map of the study area, the marine mangrove forest of Gaibu Beach, Pernambuco, Brazil.

Figure 2 .
Figure 2. Values of (A) water and air temperatures, (B) salinity, (C) pH at the marine mangrove forest of Gaibu Beach, Pernambuco, Brazil.

Table 1 .
List of the species sampled in the marine mangrove forest of Gaibu Beach, Pernambuco, Brazil.

Table 2 .
Frequency of occurrence (FO) and relative abundance (RA) of decapod crustacean species in the marine mangrove forest of Gaibu Beach, Pernambuco, Brazil.

Table 3 .
Ecological indices: monthly values of Margalef