Effect of Environmental Factors on the Abundance of Decapod Crustaceans from Soft Bottoms off Southeastern Brazil

This study investigated the importance of variations in environmental factors affecting the abundance patterns of decapods on the southeastern Brazilian coast. Sampling was carried out monthly from January 1998 through December 1999 in Ubatumirim and Mar Virado, Ubatuba region, using a commercial shrimp fishing boat equipped with double-rig nets. Six areas adjacent to rocky shores were chosen. Bottom-water samples were collected using a Nansen bottle, to measure the temperature and salinity. Sediment samples were also obtained by means of a Van Veen grab, for determination of texture and organic-matter content. The association of environmental factors with species abundance was evaluated by Canonical Correspondence Analysis (α = 0.05). Forty-one species of Decapoda were used in the multivariate analysis. The analysis indicated that sediment texture (phi) and bottom temperature were the main factors correlated (p < 0.05) with the spatial and temporal abundance of the species. Considering the study region as faunal transition zone, including a mixture of species of both tropical and subantarctic origin, the species responded differently to environmental factors, mainly temperature. It is conceivable that the decapods adjust their distribution according to their intrinsic physiological limitations, possibly as a result of the available resources.

According to Boschi (2000), the southwestern Atlantic Ocean can be divided into two provinces based on the distribution of decapod crustaceans: the Argentinian Province (from 43-44°S to 23°S), which includes the coastal waters of Patagonia, Argentina, Uruguay and Brazil (to Cabo Frio, Rio de Janeiro); and the Brazilian Province (from 23°S to 8°N), which occupies a large extent of the tropical and subtropical coast of northern and northwestern Brazil, French Guiana, Suriname, Guyana and a small part of Venezuela (to the mouth of the Orinoco River).Located on the northern coast of São Paulo State, Brazil, the Ubatuba region (23°S) is an important area for crustacean investigations.This region is a transition area between the two provinces characterized by processes of mixing and instability of the water masses (Boschi 2000), with a mixture of faunas of both tropical/subtropical and temperate origin.
The distribution limits of the majority of marine benthic organisms are determined by a complex set of environmental factors acting throughout their life cycles (Bertini et al. 2010).The presence and success of an organism or group of organisms depend on many factors.For marine benthic species, their distribution and abundance are limited by the temperature, salinity, depth, texture of the sediment, and organic matter, as well as intra-and inter-specific relationships.These environmental factors may act in isolation or together (Meireles et al. 2006).
In the region off Ubatuba (southeastern Brazilian coast), only Pires (1992) and Sumida and Pires-Vanin (1997) have studied the distribution of benthic organisms as a whole, in relation to environmental factors.The association of some individual decapods with environmental factors was examined by Fransozo et al. (1992, 1998, 2002, 2008, 2011), Negreiros-Fransozo et al. (1997), Mantelatto and Fransozo (2000), Bertini and Fransozo (2004), Castilho et al. (2008) and Bertini et al. (2010).The objective of the present study was to comprehend how variations in environmental factors (bottom temperature and salinity, sediment texture and organic-matter content) affect the abundance of decapod crustaceans inhabiting the Ubatuba region, by means of a multivariate analysis.

SAMPLING OF SPECIMENS AND ENVIRONMENTAL FACTORS
Sampling was carried out monthly from January 1998 through December 1999 in Ubatumirim and Mar Virado, located in the Ubatuba region on the northern coast of São Paulo State.Six areas adjacent to rocky shores were defined, four within bays and two near islands (Fig. 1).The samples were taken at depths of 5 m to 17 m.A GPS (Global Positioning System) was used to record the position of each sampling site.
The shrimp boat used for trawling was equipped with double-rig nets (mesh size 20 mm and 15 mm in the cod end).Each sampling area (2 Km) was trawled over a 30-min period, covering 18,000 m 2 , in the morning.
Bottom-water samples were collected monthly in each sampling area, with a Nansen bottle, to measure temperature and salinity.Temperature was measured with a mercury thermometer (°C) with accuracy of 1°C, and salinity using an optical ENVIRONMENT AND ABUNDANCE OF DECAPOD CRUSTACEANS refractometer (Atago S/1000, Tokyo), with the result expressed in parts per thousand.Only the data for bottom temperature and salinity were used in the analysis, due to the benthic habits of the decapods.
Sediment samples were obtained in each season with a 0.06 m 2 Van Veen grab, for analysis of texture and organic-matter content.In the laboratory, the sediment was oven-dried at 70°C for 72 h.For the analysis of grain-size composition, two sub-samples of 50 g were treated with 250 mL of NaOH solution (0.2 mol/L) and stirred for 5 min to release silt and clay particles.Then, the sub-samples were rinsed on a 0.063 mm sieve.The remaining sediment was again oven-dried at 60°C for 24 h and screened through six sieves of different mesh sizes.Grain-size categories followed the Wentworth (1922) American standard.The phi values were calculated, obtaining classes from -1 to greater than 4. The highest phi values correspond to the finest sediment, and the lowest values to the coarsest sediment.From the values obtained, the measures of central tendency were calculated, to determine the most frequent granulometric fractions in the sediment (Suguio 1973, Tucker 1988).The organic-matter content of the sediment in each area was estimated as the difference between the initial and ash-free dry weights of three subsamples (10 g each) incinerated in porcelain crucibles at 500°C for 3 h.

DATA ANALySIS
The relationship between the environmental factors measured and the benthic communities was analyzed by means of multivariate analysis.This statistical technique indicates broad trends in faunal composition and their association with environmental factors (Colloca et al. 2003, De Léo and Pires-Vanin 2006, Lui et al. 2007, Escobar-Briones et al. 2008, Bertini et al. 2010).
Considering the 144 trawls performed, those species with a frequency of occurrence lower than 5%, i.e., those which did not appear in at least 8 samples, were not used in the multivariate analysis, due to their low power of influence in the analysis.Thus, 41 species from the total of 80 species caught were included in the Canonical Correspondence Analysis (CCA) and cluster method.
The CCA (α = 5%), ran with the software CANOCO for Windows 4.5, was used in order to evaluate the association of the environmental variables (bottom temperature and salinity, sediment texture and organic matter) with the species abundance.Abundance data were log-transformed for the analysis, to improve their normality (Zar 1999).Cluster analysis was performed using species abundance.The species were grouped according to the Bray-Curtis similarity index, followed by the unweighted-pair group averaging (UPGMA) cluster method (Zar 1999).
All samples from both localities were incorporated into the same analysis.This approach is justified given that the goal was not to characterize each sampling location.Instead, by including the widest possible variation in environmental parameters, one would expect that the effects of these parameters on the decapod crustaceans would become more apparent.
Among the 41 species in the multivariate analysis, 9 belong to Penaeidea, 4 to Caridea, 9 to Anomura and 19 to Brachyura.The CCA revealed that all environmental factors analyzed showed a significant relationship (p < 0.05) to species abundance (Table II); sediment texture (phi) and temperature were both strongly related.The first canonical variables, when summed, explained 90.6% of the variance.The phi factor was most strongly correlated with individual abundance along the axis of the first canonical variable; and temperature was strongly correlated on the axis of the second canonical variable (Fig. 2).
The grouping analysis indicated four species groups (A, B, C and D), with approximately 20% similarity.The most abundant species during the entire study period, X. kroyeri, and the caridean shrimp Leander paulensis Ortmann, 1897 showed no similarity to the other species collected (Fig. 3).The CCA result indicated that these species showed a positive relationship with phi, on the axis  of the first canonical variable; i.e., these species were more abundant in fine sediments (Fig. 2).
Group "A" was composed by species with intermediate abundance (Fig. 3 and Table I), which were associated with coarser sediments (i.e., negatively related to phi) (Fig. 2).In addition to this relationship with the substratum, the swimming crab Portunus spinicarpus (Stimpson, 1871)  with lower temperatures (negative relationship to temperature).Subgroup "A2'1" was composed by the congener shrimps F. paulensis and F. brasiliensis.Subgroup "A2'2" was constituted by the host hermit crab Dardanus insignis (de Saussure, 1858) and symbiont porcellanid crab Porcellana sayana (Leach, 1820).Both subgroups were composed by two species with closely related life styles (Fig. 3).Species with intermediate abundance appeared in subgroup "B1" (Fig. 3 and Table I).In this subgroup, the species were associated with coarser sediments.Exception for the shrimp A. longinaris, which was correlated with finer sediments and lower temperatures; as well as the swimming crab Arenaeus cribrarius (Lamarck, 1818) and the hermit crab Loxopagurus loxocheles (Moreira, 1901), which showed no relationship to the sediment, but did show a relationship to lower and higher temperatures, respectively.Subgroup "B2" united species with low abundance and associated with higher temperatures (Figs. 2 and 3).
The majority of species with high abundance were grouped in "C" (Fig. 3 and Table I).These species showed a negative correlation with temperature and a positive correlation with phi; i.e., they were found at sites with lower temperatures and finer sediments.The exceptions to this group were the swimming crabs C. ornatus and Callinectes danae Smith, 1869, which were related to higher temperatures (Fig. 2).
Group "D" combined species with low abundance (Table I), also associated with coarser sediments.Subgroups "D1" and "D2'2" were composed by species that were mainly correlated with lower temperatures, and subgroup "D2'1" with higher temperatures (Figs. 2 and 3).
According to the CCA, the anomuran species were positively correlated with the organic-matter content (Fig. 2).
Sites with finer substrate showed a greater predominance of penaeids and some brachyuran species.The penaeids and aetrid, portunid and leucosid crabs have a burrowing habit, mainly in areas composed by fine sediments, which make burrowing easier (Dall et al. 1990, Pinheiro et al. 1996, 1997, Chacur et al. 2000, Chacur and Negreiros-Fransozo 2001, Bertini et al. 2001, Bertini and Fransozo 2004).On the other hand, the majority of brachyuran species, some hermit crabs and few penaeids were associated with coarser sediments.The finding of some burrowing species, such as the shrimps Farfantepenaeus spp., in locations with coarser sediments may be accounted for by the hypothesis proposed by Williams (1958).This author observed that in addition to a need for cover and the capacity to burrow, the respiratory requirements of shrimp may govern their burrowing habits.Substrates with a mixture of shell and sand (coarser substrate) would allow more rapid pumping during breathing than in pure beach sand or mud.This behavior indicates that shrimp adjust their burrowing not only to the ease with which they can enter the sediment but also to their respiratory requirements.
The association of hermit crabs with coarser sediment in this study is probably related to the greater availability of empty shells, because gastropods also tend to select sites with coarser sediment (Pires 1992).The availability of empty gastropod shells is a limiting resource for the survival of hermit crabs (Kellogg 1976, Negreiros-Fransozo et al. 1997), as molting hermits are exposed to predators and therefore urgently need a new and larger shell for protection.In addition, anomurans were positively related to the organicmatter content in the sediment.As mentioned by Fransozo et al. (1998), the organic content is very important in the distribution and maintenance of anomuran populations in Ubatuba Bay.Fransozo and colleagues noted that organic matter can be deposited among sediment particles or laid over the substratum as a covering layer, and that both forms are food resources available for benthic organisms.These comprise the epifauna, infauna or meiofauna, including scavenger crustaceans, and may be consumed by other benthic animals.
The Ubatuba region is influenced by three water masses with different distributional patterns in summer and winter (Pires 1992): Coastal Water (CW, Temperature > 20°C and Salinity < 36), Tropical Water (TW, T > 20°C and S > 36) and South Atlantic Central Water (SACW, T < 18°C and S < 36) (Castro Filho et al. 1987).According to Castilho et al. (2008), the intrusion of the SACW causes considerable changes to the resident communities, both positive and negative.Costa et al. (2005Costa et al. ( , 2007) ) observed a sharp decrease in bottom temperature at depths greater than 10 m, during spring and summer 1998 and 1999, probably indicating the SAWC intrusion.This scenario may explain the occurrence of cold-water indicator species such as the shrimps A. longinaris and P. muelleri and the swimming crab P. spinicarpus, as mentioned by Boschi (1963Boschi ( , 1989)), Pires-Vanin et al. (1993) and Dumont and D'Incao (2008).In this study, these species were associated with the lowest recorded temperatures and were concentrated at depths greater than 10 m.On the other hand, species with a positive relationship with temperature tend to remain in shallower waters (less than 10 m deep) during the periods influenced by cold water masses, as observed by Costa and Fransozo (2004) and Fransozo et al. (2005) for the shrimp Rimapenaeus constrictus (Stimpson, 1874) and the caridean shrimp E. oplophoroides.

ENVIRONMENT AND ABUNDANCE OF DECAPOD CRUSTACEANS
As proposed by Mantelatto et al. (2004), the occurrence of the hermit crab L. loxocheles in lower temperatures is due to the optimum of geographical distribution of this species.It is mainly distributed along the southern Brazilian and Argentinean coasts (Melo 1999), where the water is cool year-round.The same hypothesis could be proposed for the hermit crab D. insignis, which occurs from the Brazilian coast (from Rio de Janeiro down to Rio Grande do Sul) to Uruguay and Argentina (Melo 1999).
The abundance of the shrimp X. kroyeri showed only a slight positive correlation with temperature.Costa et al. (2007) suggested that during the period of SACW influx, this shrimp migrates to the northernmost part of the Brazilian southeast coast, because bottom temperatures lower than 21°C may be limiting.Xiphopenaeus kroyeri showed extremely high abundance during the study period, and thus can be considered a key species for trophic relationships of the local benthic fauna, and very important in the maintenance and equilibrium of the benthic community.
Salinity and the abundance of individuals were only weakly correlated in the present study.However, some investigators have suggested that salinity is important in the distribution mainly of certain brachyuran and penaeoid species.Of the species sampled here, the swimming crabs A. cribrarius and C. danae are euryhaline and tolerate wide salinity variations, which is necessary throughout their life cycles (Negreiros- Fransozo and Fransozo 1995, Pinheiro et al. 1996, Chacur and Negreiros-Fransozo 2001).The abundance of the shrimps F. paulensis and F. brasiliensis is also influenced by salinity variations.Costa et al. (2008), studying the distribution of juveniles of these species in an estuary in the Ubatuba region, observed that the spatial distribution of both species is influenced by salinity, but that F. paulensis is more tolerant for salinity variations than F. brasiliensis, since the juveniles of this latter species do not enter the estuary.D'Incao (1991), studying the biology of F. paulensis in the Lagoa dos Patos (Rio Grande do Sul, Brazil), one of the largest estuaries on the Brazilian coast, found only this species present in this lagoon.
Other environmental conditions besides those analyzed here, or intrinsic features of species may also modulate the distribution pattern and the abundance of benthic organisms.Fransozo et al. (2005Fransozo et al. ( , 2009)), studying the distribution of the caridean shrimps E. oplophoroides and Nematopalaemon schmitti (Holthuis, 1950) in Ubatuba Bay, proposed that the presence of marine biogenic objects (shells, carapaces, etc.) and land-derived fragments (woods, sticks, leaves, etc.) are key factors determining the presence of these species in certain parts of the bay.The crab Hexapanopeus paulensis Rathbun, 1930 is mostly found associated with plant fragments and algae, and also attached to bryozoan colonies (Bertini et al. 2004).Probably, these factors also affected the abundance of individuals in this study.
Two of the species analyzed here have a symbiotic life style: P. sayana, which is commonly found living with hermit crabs of the genera Dardanus, Petrochirus, Paguristes and Pagurus; and Minyocerus angustus (Dana, 1852), which lives in association with the sea star Luidia senegalensis (Lamarck, 1816) (Melo 1999).The abundance of these porcelain crabs is more closely related to the presence of their hosts than to the direct influence of environmental factors.
The species in the present study, some of tropical origin and others of temperate and subantarctic origin in the southwestern Atlantic Ocean, responded differently to environmental factors, according to their preferences and constraints.It is conceivable that decapod crustaceans adjust their MICHELE FURLAN et al. distribution in space and time according to their intrinsic physiological limitations, possibly as a result of available resources in tropical regions.Although water temperature and sediment type offer a most convincing explanation for the abundance patterns of the decapod crustaceans observed in this study, it is important to realize that other factors such as competition and predation may also influence their abundance.The environmental and biotic factors jointly affect the occurrence of the species, influencing their biology.These factors, together with the adaptive processes acting on each species during evolution, may explain the species' capacity to tolerate environmental changes.

ACKNOWLEDGMENTS
We thank the NEBECC co-workers for their help during the fieldwork, Dr. Janet W. Reid for her great help with English language, and the anonymous reviewers for their valuable and helpful suggestions.The authors are grateful to the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for providing financial support (#94/4878-8, #97/12108-6, #97/12106-3, #97/12107-0, #98/3134-6, #10/50188-8), and to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).All sampling in this study has been conducted in compliance with current applicable state and federal laws.

Fig. 3 -
Fig. 3 -Grouping dendrogram (UPGMA) for the species captured during the study period (January 1998 through December 1999) in the Ubatuba region.

TABLE I Data for environmental variables and the numbers of individuals of species with a frequency of occurrence greater than 5%, during the study period (January 1998 through December 1999) in the Ubatuba region.
SD: standard deviation, N: abundance, Abb: abbreviation.PE: Penaeidea, CA: Caridea, AN: Anomura, BR: Brachyura.ENVIRONMENT AND ABUNDANCE OF DECAPOD CRUSTACEANS

TABLE II Results of canonical correspondence analysis, showing the probability of significance (p) of the environmental factors.
* p<0.05.
was correlated