INTRODUCTION
Fiddler crabs of the genus Uca Leach, 1814 (family Ocypodidae) occur worldwide in the tropics and subtropics. Along the south-western Atlantic coast, ten species of fiddler crabs live on the muddy bottom of intertidal zones of bays and estuaries (Crane, Reference Crane1975; Melo, Reference Melo1996). In particular, Uca uruguayensis Nobili (1901) is distributed from Rio de Janeiro, Brazil to Mar Chiquita, Argentina (Melo, Reference Melo1996); occasionally, a few specimens can be found in locations farther south such as Puerto Quequén, Argentina (Boschi, Reference Boschi1964; Jordá & Roccatagliata, Reference Jordá and Roccatagliata2002; Roccatagliata & Jordá, Reference Roccatagliata and Jordá2002).
During the life cycle of a typical brachyuran crab, gradual or abrupt changes might occur in the shape of particular body parts and body parts whose relative size commonly change during ontogeny include the chelipeds, abdomen and pleopods. These changes are typically under endocrine control, and are related to reproductive maturation, which distinguishes the juvenile from the adult phase (Hartnoll, Reference Hartnoll1969).
The size at the onset sexual maturity (SOM) is regularly determined using allometric techniques and is useful for studies on aspects of reproduction (Vaninni & Gherardi, Reference Vaninni and Gherardi1988; Sampedro et al., 1999; Corgos & Freire, Reference Corgos and Freire2006). For instance, the morphological sexual maturity of the fiddler crab Uca cumulanta, studied by Pralon & Negreiros-Fransozo (Reference Pralon and Negreiros-Fransozo2008), showed a similar pattern to those known for other fiddler crabs, with males attaining a larger size at the SOM than females (Negreiros-Fransozo et al., Reference Negreiros-Fransozo, Colpo and Costa2003; Cardoso & Negreiros-Fransozo, Reference Cardoso and Negreiros-Fransozo2004).
Body size is probably the most important quantitative trait of an individual. It deeply affects virtually all physiological (e.g. metabolic rate) and fitness traits (e.g. fecundity or mating success), producing strong but not necessarily well understood allometric relationships within and among organisms (McNab, Reference McNab1971; Blanckenhorn & Demont, Reference Blanckenhorn and Demont2004). An increase in body size with latitude is known as Bergmann's rule (Blackburn et al., 1999). The mechanisms causing this pattern are yet to be completely understood and they relate to different hypotheses (McNab, Reference McNab1971; Blackburn et al., 1999; Blanckenhorn & Demont, Reference Blanckenhorn and Demont2004).
Apparently Bergmann's rule can be applied to decapod crustaceans. Intraspecific studies have a tendency to show that larger bodies occupy higher latitudes with a correlated increase in the size at SOM (Jones & Simons, Reference Jones and Simons1983; Hines, Reference Hines1989; Lardies & Castilla, Reference Lardies and Castilla2001; Castilho et al., Reference Castilho, Gavio, Costa, Boschi, Bauer and Fransozo2007). However, in theory, SOM should be reached by both male and female crabs at the same relative size, when they attain a specific percentage of their final body size at each locality (Charnov, Reference Charnov1990). This is evident in pandalid shrimps, where their relative size at SOM is not affected by latitude and invariably occurs at the same relative size, oscillating slightly between 0.54 and 0.56 in different localities and in seasons within localities (Charnov, Reference Charnov1990).
The fiddler crab U. uruguayensis from Brazilian and Argentinean coasts has not been studied in detail. Only a few aspects of their population biology and the occurrence of parasites have been reported (Spivak et al., Reference Spivak, Gavio and Navarro1991; Roccatagliata & Jordá, Reference Roccatagliata and Jordá2002; Costa et al., Reference Costa, Silva and Negreiros-Fransozo2006). The present study compared SOM between two populations of U. uruguayensis from different geographical regions (Brazil and Argentina). We test the hypothesis that SOM should not be affected by latitude and remains the same relative to maximum body size attained by the species at different latitudes. Also, we compared these populations to detect latitudinal effects on the relative growth pattern and the size attained by specimens.
MATERIALS AND METHODS
Both studied populations inhabit mud and sand bottom environments. In Brazil, the crabs were collected from a mangrove area in Indaiá River, Ubatuba (23o24′S 45o03′W), São Paulo, Brazil. In Argentina, the crabs were collected from a mud bank located on the mouth of a tidal creek at Punta Rasa, Samborombón Bay (36o19′S 56o47′W), Buenos Aires. Both sites are estuarine environments with very fine sediment and gentle slope. In Brazil, water temperature ranged from 15.1°C (winter) to 27.6°C (summer), and salinity from 0 to 32‰ (Colpo et al., Reference Colpo, Negreiros-Fransozo, Chacur and Guimarães2011). In Argentina, water temperature ranged from 11oC (winter) to 30oC (summer), and salinity from 18.6 to 28‰ (Guerrero et al., Reference Guerrero, Lasta, Acha, Mianzan and Framiñan1997).
Sampling was conducted during each month for one year at both localities, from January to December 2006 at Ubatuba, and from February 1995 to March 1996 at Argentina. In each area, crabs were captured manually by two collectors working for 30 minutes each, during low-tide periods (mid-intertidal) during spring tides, covering an area of 1000 m2 each month. Each collector excavated the bottom searching for the burrows and crabs inside these refuges. The use of quadrats or transects for measuring crab abundance is not appropriate in this species. Uca uruguayensis dwell among plant roots and crabs are difficult to spot in this heterogeneous habitat. In the laboratory, each specimen was sexed and the following body dimensions were measured with a digital caliper (0.01 mm): carapace width (CW); length of the propodus of the major cheliped (PL); and abdomen width, measured between the fourth and fifth somites (AW). The allometric analysis of these structures in U. uruguayensis followed that described by Benetti & Negreiros-Fransozo (Reference Benetti and Negreiros-Fransozo2004), Cardoso & Negreiros-Fransozo (Reference Cardoso and Negreiros-Fransozo2004) and Castiglioni & Negreiros-Fransozo (Reference Castiglioni and Negreiros-Fransozo2004) for other fiddler crab species.
Size comparison
The mean size of CW of U. uruguayensis was compared between the sexes and localities as well as the interaction between these two factors, using a factorial analysis of variance (two-way analysis of variance (ANOVA), sex/localities as fixed factors) (Zar, Reference Zar2010). Data were log transformed for all comparisons, but the variances remained heterogeneous (Levene P < 0.01). This procedure is considered appropriate because of the large number of samples and considering that the ANOVA test is robust enough to stand considerable departures from its theoretical assumptions (Zar, Reference Zar2010). The size of ovigerous females was compared between populations by a non-parametric Mann–Whitney U-test (Zar, Reference Zar2010) because of low sample size.
Allometric growth comparison
The relative growth analysis of the crab dimensions was based on the allometric equation (Huxley, Reference Huxley1950): y = aCW b , in which y = dimension (body structure), b = slope, which represents the relative growth rate of the body structure, and a = line intercept in the y axis. The parameters of the equation describing the relationship between the different variables were estimated by a linear regression on the log-log transformed morphometric data, i.e. the linearized equation (lny = lna + b*lnx). To determine whether the relationship deviates from linearity (b > 1 – exponential increase; b < 1 – exponential decrease; b = 1 – isometry), a t-test was used to examine whether the estimated slope b deviates from the expected slope of unity. If the body structure of the crabs grows more or less proportionally with a unit increase in size, then the slope should be greater or smaller than the unity, respectively (Hartnoll, Reference Hartnoll1978; Baeza & Asorey, Reference Baeza and Asorey2012).
Size at onset of maturity (SOM)
In order to estimate the SOM, males were first grouped into age categories according to the relationship between CW and PL. Similarly, females were first grouped into age categories according to the relationship between CW and AW. Next, a K-means non-hierarchical clustering analysis was performed. This clustering analysis distributes the data in groups of numbers previously established by an iterative process that minimizes the variance within groups and maximizes it among them. The result of the classification (K-means) was refined using discriminant analysis. This statistical methodology was based on Sampedro et al. (Reference Sampedro, González-Gurriarán, Freire and Muiño1999) and Corgos & Freire (Reference Corgos and Freire2006).
If the CW overlapped between young and adult age categories, the SOM was determined as the CW at which 50% of the specimens showed morphometric relationships that characterized the adult condition (W 50%). This value was obtained by logistic function interpolation (AP = a/(1 + be–cx)) adjusted to the data for adult proportion (AP) versus size-classes (0.5 mm) (CW). After crabs were grouped by age, the data were submitted to analysis of covariance (ANCOVA, α = 0.05), in order to test the linear and angular coefficients between groups (adult and juveniles) and between populations (Brazil and Argentina) (Zar, Reference Zar2010). The goals of this analysis were to compare the relationships of relative growth:
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– between adult and juvenile specimens, in order to detect differences occurring in ontogeny;
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– between localities for each age category, in order to assess differences between populations.
To compare the results between these populations and also to compare them with other, previously studied populations, the relative size at onset of maturity (RSOM) was calculated using the following equation:
RSOM = SOM /W∞,
in which W∞ is the asymptotic maximum size attained by crabs (Charnov, Reference Charnov1990).
As only the maximum individual sizes of each population were available, the asymptotic size was estimated by the empirical equation: W∞ = CW maximum/0.95 (Charnov, Reference Charnov1990).
RESULTS
Size comparison
Because several fiddler crab species live in the Brazilian mangroves, it is very difficult to identify specimens (at species level) smaller than 3.5 mm of CW approximately. The CW of the specimens larger than 3.5 mm CW from the Brazilian population (227 males and 123 females) ranged from 4.18 to 11.60 mm for males and from 3.90 to 9.80 mm for females (Table 1; Figure. 1). Ovigerous females (N = 8 crabs) were observed in the Brazilian population, and measured from 5.7 to 8.47 mm of CW (mean size = 7.3 ± 1.0 mm). In Argentinean estuaries the only fiddler crab species is Uca uruguayensis, and therefore all fiddler crabs found were considered to be the target species. The CW of the Argentinean specimens (259 males and 300 females) ranged from 3.60 to 14.10 mm for males and from 2.85 to 12.00 mm for females (Table 1; Figure. 1). Ovigerous females (N = 33 crabs) from the Argentinean population measured from 6.85 to 11.35 mm CW (mean size = 9.08 ± 1.28 mm). The mean size of this fiddler crab for both localities differed significantly between sexes, with males attaining larger body sizes than females (Table 2). The mean size of each sex of U. uruguayensis also differed between the populations with both males and females being larger in the Argentinean than in the Brazilian populations (Table 2).
Fig. 1. Uca uruguayensis (Nobili, 1901): size–frequency distribution of each studied fiddler crab population (A) Argentina and (B) Brazil, carapace width (mm) used as the body size representation.
Table 1. Uca uruguayensis (Nobili, 1901). Descriptive statistics and size at the onset of sexual maturity (SOM) of each studied population.
Max., maximum size; Min., minimum size; CW, carapace width (mm).
Table 2. Results of two-way analysis of variance for the carapace width between sex and localities.
df, degrees of freedom; ms, mean square.
With respect to ovigerous females, the specimens from Argentina (N = 33; 9.08 ± 1.28 mm CW) are larger than those from Brazil (N = 8; 7.3 ± 1.0 mm CW) (U = 33.5, P < 0.05).
Allometric growth comparison
Males of both populations showed positive allometry in the relationship PL versus CW for all age categories, with higher values for juveniles. When compared between populations, Argentinean males showed higher allometric coefficients for both juvenile and adult age categories (1.75; 2.05 and 1.74; 1.68 for juveniles and adults of Argentina and Brazil, respectively).
For females, the relationship AW versus CW showed the same pattern found in males, with higher allometric coefficients for the Argentinean population in both age categories (1.50; 1.29 and 1.22; 1.12 for juveniles and adults of Argentina and Brazil, respectively). Juvenile Brazilian females showed isometry even with a positive allometric coefficient (b = 1.22), this probably occurred due to the small sample size (N = 13).
The ANCOVA of transformed morphometric data (ln) revealed a statistically significant difference between the demographic categories (juveniles and adults) (Table 3) and between the populations (P < 0.05) (Table 4).
Table 3. Uca uruguayensis (Nobili, 1901). Allometric analysis of transformed morphometric data (ln) using the carapace width as independent variable, and analysis of covariance (ANCOVA) between juveniles and adults for each relationship analysed.
CW, carapace width; PL, propodus length; AW, abdomen width; AJ, juvenile specimens from Argentina; AA, adult specimens from Argentina; BJ, juvenile specimens from Brazil; BA, adult specimens from Brazil; +, positive allometry; −, negative allometry; =, isometry.
Table 4. Uca uruguayensis (Nobili, 1901). Analysis of covariance between populations for each demographic category.
CW, carapace width; PL, propodus length; AW, abdomen width; Par, parameter.
Size at onset of maturity (SOM)
An overlap of the size at maturity was found for males from the Brazilian population and for females from the Argentinean population. The SOM (W 50%) for the relationship PL versus CW for males from the Brazilian population was 7.1 mm ranging from 6.93 to 8.12 mm, while for males from Argentina the SOM was estimated at 7.0 mm CW (Table 1; Figures 2 & 3). In females, the SOM for the relationship AW versus CW was 5.9 mm for the Brazilian population, while for the Argentinean population it was 6.75 mm (W 50%), ranging from 6.2 mm to 7.5 mm CW (Table 1; Figures 2 & 3).
Fig. 2. Uca uruguayensis Nobili, 1901 in Argentina. Morphological sexual maturity: point dispersion (A) males, (B) females and (C) logistic curve (carapace width 50%) for females.
Fig. 3. Uca uruguayensis Nobili, 1901 in Brazil. Morphological sexual maturity: point dispersion (A) males, (B) females and (C) logistic curve (carapace width 50%) for males.
The RSOM was very similar for males and females from Brazil (0.58 and 0.57 for males and females, respectively) with a difference of 1% between the sexes. For males and females from Argentina, the difference between the RSOM (0.42 and 0.53 for males and females respectively) was greater (11%). Comparing between populations, lower values were found for crabs in Argentina, with a difference of 16% for males. For females the difference was small (3%).
DISCUSSION
Body size and sexual dimorphism
The size of the fiddler crab Uca uruguayensis showed latitudinal cline, corroborating the Bergmann's rule, with the smaller crabs occurring at the lower latitude (Brazil) and larger crabs at the higher latitude (Argentina). There is much debate as to whether the ectothermic Bergmann cline is adaptative and/or a mere consequence of physiological processes (Blanckenhorn & Demont, Reference Blanckenhorn and Demont2004). However, at the moment, there is no general theory available demonstrating the adaptive nature of Bergmann clines (Atkinson & Sibly, Reference Atkinson and Sibly1997; Blanckenhorn & Demont, Reference Blanckenhorn and Demont2004). In contrast, physiologists emphasize different mechanisms to explain the Bergmann's rule. These mechanisms are normally related to different thermal exposures that could result in different physiological costs at the cellular level (Stillman & Somero, Reference Stillman and Somero2000). The theoretical basis for clarifying the hypotheses and mechanisms involved in the Bergmann's rule was previously discussed by Blackburn et al. (Reference Blackburn, Gaston and Loder1999) and Blanckenhorn & Demont (Reference Blanckenhorn and Demont2004).
Males were larger than females in both populations. This is commonly found for brachyurans (Warner, Reference Warner1967; Benetti & Negreiros-Fransozo, Reference Benetti and Negreiros-Fransozo2003; Johnson, Reference Johnson2003; Luppi et al., Reference Luppi, Spivak, Bas and Anger2004; Litulo, Reference Litulo2005; Hirose et al., Reference Hirose and Negreiros-Fransozo2008) and is probably related to sexual selection based on the reproductive behaviour of these crabs. In fiddler crabs, males have one of their two chelipeds greatly enlarged. It lost its feeding function and is used in both fighting and visual displaying (waving), which consists of a rhythmic elevation and lowering of the major chelae in order to attract the females into the male's burrow during the breeding season (Crane, Reference Crane1966, Reference Crane1975; Yamaguchi, Reference Yamaguchi1977; Latruffe et al., Reference Latruffe, MacGregor and Oliveira1999). The CW of males of this species is usually correlated with their claw size (Hyatt & Salmon, Reference Hyatt and Salmon1978) and, consequently, larger males can have an advantage in male–male competition. Larger body and claw may also have an adaptive value in mate attraction, where an enlarged and conspicuous claw would provide an advantage as it would be more easily detected and/or attractive to the wandering female (Oliveira & Custódio, Reference Oliveira and Custódio1998).
An extended period of somatic growth and/or a greater moult increment may also reflect differences in body size between males and females. The energy allocated to reproduction should be proportionally higher in females, because more energy is needed for the production of oocytes than that of spermatocytes, and thus females can interrupt or reduce their somatic growth while they are incubating eggs (Alunno-Bruscia & Sainte-Marie, Reference Alunno-Bruscia and Sainte-Marie1998; Hartnoll, Reference Hartnoll2006). Slower growth can also reflect a reduced energy intake because of feeding restrictions. In females, a more general phenomenon is a restricted feeding habit during incubation. A further limitation on the growth of reproducing females is that they cannot moult while incubating eggs (Hartnoll, Reference Hartnoll2006).
Males of both populations, showed a higher allometric coefficient value (b) for the cheliped, during the juvenile phase. This may be a very important growth strategy and might be a response, in part, to the differences in the relative size of morphological sexual maturity for males between the populations. Behaviour in this genus is predominantly visual (Crane, Reference Crane1975), and rapid development of the chelipeds may also ensure that a male could more rapidly and effectively participate in reproductive processes, and interact with other males for territory and/or food (Christy, Reference Christy1978, Reference Christy1983; Christy & Salmon, Reference Christy and Salmon1984; Backwell et al., Reference Backwell, Christy, Telford, Jennions and Passmore2000). Large claws and the waving activity of males are important criteria for mate selection and it is primarily directed at receptive females (Oliveira & Custódio, Reference Oliveira and Custódio1998; Latruffe et al., Reference Latruffe, MacGregor and Oliveira1999).
There was a marked difference between the sexes with respect to the abdomen. In females, the abdomen growth showed high values of positive allometry. This growth pattern is related to the protection of the gonopores and egg mass during incubation and to the increase in the incubation capacity (Hartnoll, Reference Hartnoll and Abele1982).
Both populations showed a similar growth pattern, with positive allometric growth (see Table 2, and Figures 2 & 3). However, within the Argentinean population, a higher allometric coefficient (b) was found for both sexes, mainly in juveniles. This could indicate different strategies for growth and reproduction between populations from different latitudes. An increase in the allometric growth coefficient of the secondary sexual appendages could anticipate the relative size at the onset sexual maturity (or RSOM), and consequently change the longevity and the life-time investment in reproduction (Anger & Moreira, Reference Anger and Moreira1998).
Morphological sexual maturity
The size at onset of the sexual maturity (SOM) of the two populations was estimated and compared based on the allometric technique. SOM was very similar for both (Brazilian males = 7.1 mm; Brazilian females = 5.9 mm; Argentinean males = 7.0 mm; Argentinean females = 6.75 mm CW). Considering the small number of juvenile Brazilian females used in the analysis of maturity, a bias should be expected. However, when comparing the size of the smallest ovigerous female (5.7 mm CW) with the estimated size at morphological sexual maturity (5.9 mm CW), it becomes clear that the values are quite close, and therefore we consider the estimate valid.
The relative size of SOM (RSOM) was lower for males and females of U. uruguayensis from the higher latitude (36oS) (RSOM = 0.42 and 0.53, respectively) than for those from the lower latitude (23oS) (RSOM = 0.58 and 0.57, respectively). These differences found in the RSOM are not surprising since the allometric growth coefficient of the secondary sexual appendages was higher in the Argentinean than in the Brazilian population. These results reinforce the hypothesis proposed by Pralon & Negreiros-Fransozo (Reference Pralon and Negreiros-Fransozo2008) that this parameter is not a constant among the genus Uca. Conde & Díaz (Reference Conde and Díaz1992) suggest that the intraspecific variation in the relative size at the SOM can be a reflex of a great plasticity of the species under different environmental conditions.
The correlations of the body size with latitude of U. uruguayensis demonstrated by a latitudinal cline, reinforces the ecogeographical rule initially proposed by Bergmann. This pattern is common in many arthropods, although the underlying cause of the Bergmann rule to date remains a mystery (Blanckenhorn & Demont, Reference Blanckenhorn and Demont2004). Regarding the relative size at which U. uruguayensis attained sexual maturity in different habitats, our results contrast with the null hypothesis tested. This is probably because the life history features of U. uruguayensis are very plastic under different environmental conditions, i.e. different levels of productivity and stress, or the presence, mainly in mangrove areas, of large amounts of growth-inhibiting substances (e.g. polyphenols derived from tannins of halophyte plants) (Power & Bliss, Reference Power, Bliss and Bliss1983; Rodríguez, Reference Rodríguez1987; Díaz & Conde, Reference Díaz and Conde1988, Reference Díaz and Conde1989; Conde & Díaz, Reference Conde and Díaz1989; Negreiros-Fransozo, Reference Negreiros-Fransozo, Escobar Briones and Alvarez2002). Other studies comparing the population parameters at different latitudes are needed for a better understanding of the life-history variants of the South Atlantic fiddler crabs.
ACKNOWLEDGEMENTS
We thank the CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) and the Graduate Course in Zoology at the ‘Instituto de Biociências, Universidade Estadual Paulista' for financial support for this research and also the visit of Laura S. López-Greco from Argentina to Brazil (Prosul #490208/2005-3). We also thank Drs Daniel Roccatagliata and Martín Torres Jordá from the ‘Facultad de Ciencias Naturales y Exactas, Universidad de Buenos Aires' for donation of Argentinean specimens and Dr Janet W. Reid for improving our English. All sampling in Brazil was carried out according to state and federal laws regulating wildlife collection.
