Clibanarius symmetricus (Randall, 1840)

Melo, Ana Carolina, Rodriguesb, Melo & Martinelli-Lemos, Jussara Moretto, 2019, Spatiotemporal distribution and population structure of Clibanarius symmetricus (Randall, 1840) (Crustacea, Diogenidae) in an Amazon estuary, Turkish Journal of Zoology 43 (5), pp. 490-501 : 495-499

4.1. Spatiotemporal distribution of C. symmetricus

The distribution of C. symmetricus in the Marapanim estuary is influenced directly by environmental factors such as temperature, which may influence a number of aspects of the biology of the species, such as reproduction and growth patterns, and sexual maturation. The variation in crab density found between seasons and in the different sectors and zones of the Marapanim estuary during different periods reflects the spatiotemporal variation in environmental factors.

While no significant correlation was found between the density of crabs and salinity in the present study, the abundance of C. symmetricus was greatest where the water was most saline. Sant’Anna et al. (2009) found evidence that salinity may have an important influence on the reproductive patterns of this species. Although no data are available on the influence of salinity on the development of C. symmetricus larvae, high salinity is known to be a requirement for the adequate development of the eggs and larvae of Clibanarius vittatus (Fotheringham and Bagnall, 1976; Lowery and Nelson, 1988; Kelly and Turner, 2011). Given the observations in the present study, it would be reasonable to assume that C. symmetricus may also require more saline environments, which would restrict its presence in the inner sectors of the estuary. In a study of anomuran larvae in the Marapanim estuary, Oliveira and Martinelli-Lemos (unpub. data) found a positive correlation between the density of these organisms and salinity, with higher densities being recorded in the lower estuary, adjacent to the open sea. While all the evidence points to a preference for more saline conditions, the lack of a significant correlation in the present study may be related to the small numbers of larvae collected.

specimens collected in the Marapanim estuary, Pará, Brazil (SD: standard deviation).

One other factor that may limit the presence of these organisms to the lower estuary is the sediment. As the lower estuary has rock fragments of larger size ( Silva and Martinelli-Lemos, 2012), this may favor the occurrence of the organisms by providing refuge from high temperatures and the physical stress of breaking waves. This may also account for the higher density of C. symmetricus recorded in the lower midlittoral zone, which is less exposed to the sun during the tidal cycle than the upper zone, where relatively high temperatures may cause heat stress and increase the risk of desiccation.

In addition to providing protection, rocky substrates provide a wider variety of microhabitats, in which many organisms that provide nutritional resources can be found ( Fransozo et al., 2008). The rocky outcrops of the estuaries of the Amazon coast harbor a wealth of decapod crustaceans ( Oliveira et al., 2012; Silva and Martinelli-Lemos, 2012; Oliveira et al., 2013; Morais and Lee, 2014; Sampaio and Martinelli-Lemos, 2014; Rodrigues and Martinelli-Lemos, 2016; Nóbrega and Martinelli-Lemos, 2016), which may create an environment favorable for the development of hermit crabs.

The variation in temperature in the study region is small; however, the density of C. symmetricus was correlated negatively with water temperature. Hermit crabs may suffer considerably from heat stress in this environment, and during hotter periods, they may actively seek out a cooler environment. Sant’Anna et al. (2009) considered temperature to be an important factor in determining the reproductive patterns in this species, as well as acting as a regulator of metabolic and biochemical activity, and a hormonal cue.

The hermit crab C. symmetricus was least abundant at site A2 (western margin, middle estuary). In addition to the site having less-saline waters, the substrate at this site—small rocks partially covered by mud—appears to be less favorable to the species. The site is also influenced by the presence of urban development, i.e. the town of Marapanim and the village of Marudá, which are not only residential areas but also function as centers of tourism, especially during vacation periods, further intensifying the potential impact on the structure of the C. symmetricus populations found in this area.

Overall, then, the evidence implies that C. symmetricus tends to occur in areas with more saline water, substrates with larger rocks, and less anthropogenic impact. Migration patterns may be related to the need to find optimal locations for development. Fotheringham (1975) first highlighted the influence of seasonal and reproductive factors on migratory behavior; hermit crabs may also migrate in search of important resources such as appropriate empty shells (see Gherardi et al., 1990).

The availability of gastropod shells and competition for this resource are also important factors influencing the distribution of hermit crab populations ( Hazlett, 1981; Martinelli and Mantelatto, 1999; Bertini and Fransozo, 2000; Fransozo et al., 2008), including C. symmetricus ( Sant’Anna et al., 2006b; Rodrigues and Martinelli-Lemos, 2016). Variation in the availability of food sources and the feeding behavior of the crabs may also have an important influence on the large-scale distribution of C. symmetricus ( Dunbar et al., 2003) .

4.2. Population structure of C. symmetricus

Ovigerous C. symmetricus females were relatively rare overall (1.74% of total abundance); however, as they were not absent altogether, reproduction does appear to be occurring in the population. It seems likely that most ovigerous females may have migrated to locations closer to the mouth of the estuary than the outermost sampling points surveyed in the present study (sites A1 and B1) Χ 2 = chi-square; P = probability (α = 0.05). Significant values are highlighted in bold.

* In January, only intersex and undetermined individuals were encountered.

in search of more saline water and more appropriate substrates (larger rocks), as well as optimal salinity for spawning ( Sant’Anna et al., 2009).

The relative rarity of intersex individuals (5.57%) appears to be a common feature of C. symmetricus populations throughout its geographic range. Turra and Leite (2000) found that 5%–7% of a population in a subtropical region was intersex, and even lower frequencies have been recorded in other tropical and subtropical areas, with Sant’Anna et al. (2009) recording a frequency of 2.5%, Sampaio et al. (2009) recording one of 1.9%, and Mantelatto et al. (2010) only 0.3%.

Intersex individuals were long considered to be functional males, given that female sexual features are only present in the external morphology ( Turra, 2004), until Turra (2007) found an ovigerous intersex individual. Ovigerous intersex individuals were also collected in the present study, indicating that they may also be functional females. Intersexuality may thus represent a form of hermaphroditism involving the simultaneous presence of both female and male gonads in the same individual ( Sant’Anna et al., 2010), although this requires further investigation.

The sexual dimorphism recorded in the present study population is consistent with that found in the species at other latitudes ( Reigada and Santos, 1997; Turra and Leite, 2000; Sampaio et al., 2009; Sant’Anna et al., 2009; Mantelatto et al., 2010). Sexual dimorphism appears to be a characteristic common to all hermit crabs (e.g., Mantelatto and Martinelli, 2001; Bertini et al., 2004; Biagi et al., 2006a; Ayres-Peres and Mantelatto, 2008; Fantucci et al., 2009). This may be related to the difference in energy available for growth, with males having more energy available for somatic growth in comparison with females, who must dedicate more energy to the production of eggs. Larger males may also be able to outcompete smaller males in mating combats, and thus gain access to more reproductive partners, as described by Abrams (1988).

Morphological sexual maturity estimated from the analysis of relative growth patterns shows smaller size than that recorded in tropical and subtropical regions ( Table 4). Relative growth is often used to determine sexual maturity in hermit crabs, and is considered a reliable criterion for this purpose ( Biagi et al., 2006b). The earlier sexual maturity recorded in the present study may be related to the higher temperatures found in the equatorial Marapanim estuary, which may favor growth and development. The Bergmann rule, which explains latitudinal body size variation in vertebrates (later adopted to invertebrates), postulates that animals at higher latitudes tend to be larger in size to better tolerate colder temperatures ( Bergmann, 1847). As reproductive potential is defined by the body size and rate of growth of an organism, reproductive age will decrease with decreasing growth rates ( Giesel, 1976).

A nonnormal, unimodal distribution of body size has also been recorded in C. symmetricus in other regions (Sant’Anna, et al. 2009; Mantelatto et al., 2010). The presence of juvenile individuals throughout the year reflects a continuous reproductive process in the present study population. The high frequency of juveniles recorded in the present study indicates that they inhabit the same areas as the adults, in contrast with the findings of Sant’Anna et al. (2009), who reported that the adults inhabited an area distinct from that of recruitment. This indicates that the Marapanim estuary is suitable for the development of the entire population, making it an important site for the conservation of C. symmetricus .

Mantelatto et al. (2010) also recorded continuous reproduction in a population in tropical northeastern Brazil, which indicates that this may be the typical pattern for C. symmetricus in tropical and equatorial regions. In subtropical regions, however, seasonal breeding is the norm ( Turra and Leite, 2000; Sampaio et al., 2009; Sant’Anna et al., 2009; Mantelatto et al., 2010). This indicates that the breeding pattern of these hermit crabs varies by latitude, as observed by van de Kerk et al. (2016), who concluded that the reproductive strategies of a species, such as its breeding frequency, may vary along a latitudinal gradient.

A male-biased sex ratio has been recorded in C. symmetricus populations in southern ( Sampaio et al., 2009) and southeastern Brazil ( Mantelatto et al., 2010). However, a female-biased sex ratio was recorded in C. symmetricus populations in southeastern ( Negreiros-Fransozo et al., 1991; Turra and Leite, 2000; Sant’Anna et al., 2009) and northeastern Brazil ( Mantelatto et al., 2010). A male-biased sex ratio may be the result of differential survival or life expectancy, but may also represent an adaptive strategy that permits each female to mate with more than one male ( Ayres-Peres and Mantelatto, 2008). Other determinants may include differential sexual migration ( Wenner, 1972). This may have been a factor in the present study, given