Temporal distribution in the abundance of the fiddler crab Uca ( Leptuca ) uruguayensis Nobili , 1901 ( Decapoda : Ocypodidae ) from Garças River mangrove , Guaratuba Bay , southern Brazil

A study on the temporal distribution, sex ratio, reproductive period, recruitment of juveniles and size composition of individuals of the fiddler crab Uca (Leptuca) uruguayensis was carried out in a population living in the Garças River mangrove, Guaratuba Bay, Paraná State, Brazil. Eight square samples of 0.25 m2 (0.50 m side) were obtained on a monthly basis, from April/2011 to March/2012. The crabs were collected through the excavation of burrows and their carapace width (CW) was measured. Air and water temperatures varied from 19.0 to 29.5°C and 17.0 to 27.0°C, respectively, the salinity from 7 to 23 and the soil temperature from 19.0 to 29.2°C. A total of 1,099 fiddler crabs were collected, being 529 males, 520 females (of these, 9 ovigerous) and 50 sexually undifferentiated individuals. The average density of the population ranged from 12 (June/11) to 71 ind.m-2 (May/11), but its annual fluctuation was not correlated to abiotic variables. The sex ratio was 1:1 all year round and in all CW classes. Although in low abundance, ovigerous females were recorded in six months and juvenile crabs were present all year round, indicating a continuous reproduction and recruitment of the species. The CW of males ranged from 2.33 to 8.33 mm and that of females, from 2.52 to 7.79 mm: these data showed that this population is composed of smallest individuals among those studied.


INTRODUCTION
Uca (Leptuca) uruguayensis Nobili, 1901 is one of the ten species of fiddler crabs recorded in Brazil (Bezerra, 2012). It is distributed in Western Atlantic, from Rio de Janeiro (Brazil) to the mouth of the Quequén River in the province of Buenos Aires (Argentina) (Boschi, 2000). The species is associated with mangrove ecosystems in most of Brazilian coast of its distribution (Branco, 1991;Melo, 1996), or with estuarine marshes in the coast of southernmost Brazil, Uruguay and northern Argentina (Spivak et al., 1991).
Many aspects have been investigated on the populations of U. (L.) uruguayensis from The population of U. (L.) uruguayensis living in the Guaratuba Bay, Paraná Sate, was the third most abundant with a maximum density of 84.0 specimens.m -2 in the collection site where the organic matter content was very high (10.43%). It has euryhaline habit and occurred in almost all collection sites in this bay (Masunari, 2006). In the Garças River mangrove (Guaratuba Bay), these crabs occur mainly in sunny banks along streams that run inside it (Martins and Masunari, 2013).
This paper aims to describe the temporal oscillation of density and population structure of U. (L.) uruguayensis during a period of twelve months, in the Garças River mangrove, Guaratuba Bay, Paraná State, Brazil. The following aspects were treated: the annual fluctuation of density and sex ratio, reproductive period, recruitment of juveniles and the size composition of individuals.

MATERIAL AND METHODS
The study was conducted along the riverbank of the Garças River (25° 53'S, 48° 38'W) located in the southern portion of the Guaratuba Bay, Paraná State, Brazil (Fig. 1). The area is dominated by relatively well preserved mangrove and it belongs to the Boguaçú State Park. For further details of the study area see Martins and Masunari (2013).
The collections were carried out monthly during spring low tides, from April/2011 to March/2012. Temperatures of the air, water and soil (at surface and depths of 15 and 25 cm), and the water salinity were measured in each collection. The monthly average temperature and precipitation were provided by SIMEPAR, a weather station in the municipality of Guaratuba, Paraná State.
Monthly, crabs were collected from eight quadrats (0.25 m 2 ) randomly placed within a 24 m² soil surface of marginal sunny banks. All open burrows contained inside these quadrats were inspected and the crabs were manually collected with the aid of a small garden spade. The collected crabs were kept in plastic bags and transported in ice box to avoid losing appendages until arrival in the laboratory, where they were fixed in formalin and preserved in 75% ethanol for further analysis. In the laboratory, the crabs were identified, sexed, checked for the presence of eggs and the carapace width (CW) was measured between the antero-lateral angles with the aid of a digital microscope (Dino-Lite Pro AM-413T). These specimens were deposited in the Museum of Natural History of Capão da Imbuia (Curitiba, Parana State, Brazil), under No 3561 to 3651.
The density of crabs was expressed by the number of individuals per square meter (n°. ind.m -2 ). The period of time when ovigerous females were found in the population was considered as the main breeding period. Those crabs without visible sexual dimorphism were considered as "sexually undifferentiated individuals" (SUI). Crabs SUI and those with less than 4.14 mm CW for males and less than 3.52 mm CW for females were collectively called juveniles, based on the study of relative growth of U. (L.) uruguayensis from the same collection site (Martins and Masunari, 2013).
The difference in the oscillation of the soil temperature at various depths was analyzed with unifactorial analysis of variance (ANOVA). The Spearman test was used to check for correlations between the density of the population of U. (L.) uruguayensis and the measured abiotic variables. The sex ratio was evaluated using the chi-square test (c 2 ) for an expected proportion of 1:1, with a confidence level of 95%. The differences in the absolute number of juveniles between the seasons were tested using Kruskal-Wallis. Mean size of males and females was compared using the Mann-Whitney test. The Shapiro-Wilk test was used to test the normality of frequency distributions (Zar, 1996).

RESULTS
Air temperatures measured in the field ranged from 19.0 (July/11) to 29.5°C (March/12), and the monthly average temperatures fluctuated from 16.6 to 25.7°C (SIMEPAR) (Fig. 2), the water temperatures ranged from 17.0 (June/11) to 27.0°C (March/12), following the same pattern observed that the air temperatures, except May/11 and December/11, when the values were below the respective monthly average air temperatures (not shown in figure).
The temperatures of soil surface oscillated from 20.9 (September/11) to 29.2ºC (February/12). Soil temperatures at 10 cm and 20 cm depth varied respectively from 19.0 (September/11) to 28.0°C (February/12) and 19.0 (September/11) to 27.9°C. Soil temperatures did not differ significantly between the three depths (p > 0.05). In general the soil temperatures (depth averages) followed the variation of air temperature (monthly averages).
The monthly rainfall ranged from 103.0 mm to 428.6 mm in the Guaratuba region (SIMEPAR) (Fig. 2), while the salinity of the river water fluctuated from 12 (August/11 and January/12) to 23 (June/11) in most months, but there was a sudden reduction in 7 (September/11 and October/11) and 9 (December/11), when a strong rainfall took place in the days before the collections. There was no correlation between salinity and monthly rainfall oscillations (r² = 0.1921 and p > 0.05).

Sex ratio
The overall sex ratio was 1:1 and did not differ significantly from the expected proportion (c 2 test = 0.077, p > 0.05). The same sex ratio was found in all months ( Fig. 3 and Tab. 1) and in all CW classes (Fig. 4).

Reproductive and recruitment period
A total of nine ovigerous females were collected in April/11 (n = 5), July/11 (n = 1), September/11 (n = 1), October/11 (n = 1) and March/12 (n = 1) (Fig. 5). The juveniles were present in all sampled months indicating a continuous recruitment, with higher abundance in winter (July, August and September, n = 138) followed by summer (January, February and March, n = 59), autumn (April, May and June, n = 57) and spring (October, November and December, n = 49). The highest frequency of ovigerous females recorded in autumn was followed by the season of highest frequency of juveniles (winter) (Fig.  5). There was a statistically significant difference in the frequency of juveniles between winter and summer (Kruskal-Wallis; H = 11.0578; p < 0.05), winter and spring (Kruskal-Wallis; H = 11.0578; p < 0.05) and winter and autumn (Kruskal-Wallis; H = 10.6936; p < 0.05), but a continuous recruitment throughout the year is evident (Fig. 5).

Temporal distribution in the density
The oscillation of the average density of the population was not related to the abiotic variables' in the present study. However, the lowest density occurred in the winter, in the month (June) of lowest water temperature (17°C) and the second lowest average air temperature (16.9°C).
Likewise, in Mar Chiquita, Argentina (Spivak et al., 1991) the abundance of U. (L.) uruguayensis was not related to air/ water temperatures: the highest (August, ≈ 40 ind.m -2 ) and lowest (April, ≈ 4 ind.m -2 ) densities occurred in different months from the present study (71 ind.m -2 in May and 12 ind.m -2 in June). Later, César et al. (2005) obtained the maximum density in February (42 ind.m -2 ) and the minimum in July (0 ind.m -2 ) for the population from Samborombón Bay, Argentina, showing a significant correlation with water temperature and salinity oscillations: the higher densities were recorded in spring and summer while the smaller ones in the colder seasons (autumn and winter).
This pattern was also observed by Branco (1991) in the mangroves of Itacorubi (Santa Catarina State), Brazil, where the maximum abundance was recorded in spring, (n = 270) and the minimum in winter, (n = 25). Anyway, it seems that U. (L.) uruguayensis reduces its activities during cold months in regions with marked oscillation of air temperature, resulting in low densities in cold months, in spite of different methodologies of collection of crabs: by excavation performed by Spivak et al. (1991), by capture of crabs walking on the surface by Branco (1991), or by inspection of burrows (present study).
The lack of relationship between the oscillation of density and that of temperatures highlights the eurythermic nature of U. (L.) uruguayensis, that could stand a 10.5°C range of average monthly temperatures (from 19.0 to 29.5°C). Within this oscillation range of average air temperature, most of these crabs in Guaratuba Bay, are able to opening burrows throughout the year.
In contrast, the abundance of U. (L.) uruguayensis from Samborombón Bay, Argentina, showed a significant correlation with water temperature and salinity, higher densities being recorded in the warmer season and higher water salinities, while the lowest ones in colder seasons and low salinities (César et al., 2005). Another difference in the population parameter was the density: while in the population of Argentina, it varied from 0-42 ind.m -2 , in the present study, it ranged from 12-71 ind.m -2 . This difference may be connected to the contrasting size of these crabs: the male crabs of Argentina population measure up to 14.47 mm CW (Spivak et al., 1991), while those of the Guaratuba Bay, 8.33 mm CW (Martins and Masunari, 2013).
The euryhaline nature of Uca (L.) uruguayensis observed in the present study (it stands salinity range of 16, from 7 to 23) is in accordance to Masunari (2006) for other populations from the same estuarine area, where salinities varied from 7.92 to 23.64. However, these salinity ranges are quite narrow if compared to Uca (Minuca) longisignalis Salmon and Atsaides, 1968 and Uca (Minuca) subcylindrica Stimpson, 1859 from the semiarid regions of Texas, USA: they support salinity variations in the laboratory from 2.0 to 90.0 and 0.08 to 110.0, respectively (Rabalais and Cameron, 1985).

Sex ratio
The sex ratio found in this study (1:1) is in accordance with César et al. (2005) with the population from Samborombón Bay, Argentina, but different from that found by Bedê et al. (2008) in the mangrove of Itacuruçá, Brazil (1:0.42) and from Mar Chiquita, Argentina (1:1.68) (Spivak et al., 1991).
Other factors may also cause deviations in the expected sex ratio as the differences in the food availability for females and males, habitat fragmentation, spatial use of resources and differential migration patterns (Wilson and Pianka, 1963;Giesel 1972;Wolf et al., 1975;Christy and Salmon, 1984;Montague, 1980;Genoni, 1985;Spivak et al., 1991;Costa and Negreiros-Fransozo, 2002).
The mendelian sex ratio observed in the population of U. (L.) uruguayensis from the Garças River mangrove may indicate that males and females are under similar conditions (e.g. food availability, predation pressure).

Reproductive period and recruitment
The low frequency of ovigerous females recorded in this study probably was due to their reclusive habit for protecting themselves against unsuitable conditions. This inference is supported by the general behavior of the ovigerous females of large front fiddler crabs, to which U. (L.) uruguayensis belongs, that they stop feeding and incubate their eggs inside the burrows (Crane, 1975;Murai et al., 1987;Christy and Salmon, 1991). Actually, Costa et al. (2006) observed ovigerous females of this species living in deep burrows, confirming the statement of the above authors. This strategy is perceived in order to protect the egg mass against extreme environmental conditions, enabling a synchronism on the embryonic development and larval hatching (Salmon, 1987).
Although in very small frequency, ovigerous females were present in all seasons at the Guaratuba Bay as observed at Fortaleza Bay, São Paulo State, Brazil by Costa et al. (2006). These data may suggest that U. (L.) uruguayensis has continuous reproduction at least for populations living in latitudes lower than Paraná State, Brazil. On the other hand, in the studies carried out by César et al. (2007) in the Samborombón Bay and by Spivak et al. (1991) in Mar Chiquita, in temperate climate in Argentina, it was observed that reproduction is seasonal (spring and summer).
The higher number of juveniles in the winter months of the present study could be produced by ovigerous females that were more numerous in Autumn months (Fig. 5), in spite of the low frequency of these females. This assumption is based on the observation of Costa and Negreiros-Fransozo (2002) with population of U. (M.) thayeri from São Paulo State coast, and of Castiglioni et al. (2006) with population of U. (M.) rapax from Rio de Janeiro State, both in Brazil.

Population structure in carapace width
The slight predominance of females (without statistical differences in the number of males and females) in the smaller CW classes and of males in the larger ones of the present study may be explained by differential growth in males and females. These females have two main events that may slow or stop their somatic growth: part of their energy is directed to gonadal development and for the supply during egg laying (Warner, 1967;Díaz and Conde, 1989;Johnson, 2003) and they hardly feed during the egg incubation (Crane, 1975;Christy and Salmon, 1991). On the other hand, males can grow continuously attaining larger size for courtship purposes (Warner, 1967;Adiyodi and Adiyodi, 1970;Wenner, 1972;Christy and Salmon, 1984;Díaz and Conde, 1989;Henmi and Kaneto, 1989). This observation was also reported by Bedê et al. (2008) in the population of U. (L.) uruguayensis from Rio de Janeiro State coast. As mentioned above, males and females of U. (L.) uruguayensis from the Guaratuba Bay are under the same predation pressure, unlike other Uca species (Ribeiro et al., 2003).
The unimodal distribution of CW classes for both sexes in the present study was different from the population of Rio de Janeiro State coast where a bimodal distribution for females was recorded (modal CW classes in 5.0 to 6.0 mm and in 7.0 to 8.0 mm) (Bedê et al., 2008). These authors explained this exceptional feature as a consequence of the small number of female samples (n = 24).
The size frequency distribution of a population is a dynamic feature that can change throughout the year as a result of the reproduction and juvenile recruitment (Thurman, 1985). The unimodal distribution observed in the present study suggests a stable population, with continuous and constant recruitment and mortality rates throughout the life cycle, a pattern common to other species of Uca, mainly of tropical regions (Díaz and Conde, 1989;Litulo, 2004;2005).
The CW values for both sexes obtained in the present study are noteworthy for their smallness. The population of the Guaratuba Bay is composed of the smallest individuals (males 2.33 to 8.33 mm, non-ovigerous females 2.52 to 7.79 mm and ovigerous females 5.05 to 6.95 mm). The population from Itacuruçá mangrove, Rio de Janeiro, measured 4.57 to 12.00 mm (males) and 5.00 to 10.86 mm (females) (Bedê et al., 2008), from Indaiá River mangrove, São Paulo, measured from 4.18 to 11.60 mm (males) and 3.90 to 9.80 mm (females) (Hirose et al., 2012), and from Argentina, maximum CW values measured were 14.47 mm (males) and 13.43 mm (females) (Spivak et al., 1991) and 14.10 mm (males) and 12.00 mm (females) (Hirose et al., 2012). Differences in food availability seem to be the main cause for this strong CW discrepancy among populations from different localities (Colpo and Negreiros-Fransozo, 2004). Future investigations would confirm this hypothesis.
Despite the small size of the individuals that compose the population of U. (L.) uruguayensis at the Garças River mangrove, there are indications that it is well established as pointed out by the presence of all demographic categories throughout the year especially of ovigerous females and juveniles.