Neohelice granulata burrow fidelity behaviour related to landscape heterogeneity

The low recovery rates for tagged crabs observed at all sites indicate that the semiterrestrial crab N. granulata displays low fidelity during its daily activity pattern (after 48 h less than 1% for all study populations, Table 1). In a previous work on this species [25] it has been reported that individuals can show a high mobility rate between different patches (saltmarsh and mudflat) in short periods of time (e.g. along of tidal cycle) and this is probably related to the use of different types of habitats to eating, resting and reproducing, as it was also observed in ecologically equivalent species (such as A. cinereum) [52]. This high rate of mobility that crabs in N. granulata exhibit could explain the low fidelity we found here. N. granulata uses two dominant feeding strategies (detritivorous and herbivore) that are context-dependent; when habitats are covered by tides crabs predominantly feeds on leaves of Spartina sp. [53] while when the tide withdraws they feed mud [54] which could lead to higher rates of migratory movements during high tide [25].

Stachowicz and Hay [16] proposed that crabs with generalist feeding habits exhibit reduced mobility and strong fidelity behaviour to a particular area. Despite the fact that N. granulata has an omnivorous–detritivorous feeding habit [54, 55] our data indicate that site fidelity in N. granulata is weak. Low burrow fidelity has also been observed in other marsh Graspid species such as S. reticulatum, A. cinereum and Hemigrapsus sanguineus [14, 51]. Similarly to N. granulata, these species show “unfaithful” daily behaviour, being capable of travelling long distances within their habitat [14, 56], as well as having omnivorous–detritivorous feeding habit [56, 57] indicating that the Stachowicz and Hay’s model cannot be applied.

The strength of site fidelity for burrow holding may be a function of the costs and benefits incurred by different strategies such as (1) constructing a new burrow, (2) acquiring and restoring an unoccupied burrow, or (3) continuously maintaining and defending the individual’s own burrow. In addition, even when the time and energy required to dig a new burrow may be negligible, the availability of free appropriate space to dig a new burrow or the likelihood of finding an unoccupied one may be some of the variables that influence which strategy is chosen. For example, fiddler crabs are known to have strong site fidelity [58] to their burrows, which they use as a refuge during both high and low tides, as protection from physiological stress [59] and a place for mating [60]. With some exceptions [20], fiddler crabs feed on the sediment located within a radius that rarely extends beyond 1 m from the opening of their burrows [61]. During feeding bouts, fiddler crabs are constantly retracting in response to any predation risk or any attempted theft by an intruder [8, 58]. In fiddler crabs, the likelihood of finding an unoccupied burrow may be low because unoccupied burrows that are not plugged are irretrievably crumbled and destroyed by the incoming tide. In addition, coalitions between neighbours [62] may prevent burrowless crabs from digging new burrows in their neighbourhood, forcing them to marginal areas. Therefore, losing or discarding a burrow may be more costly for fiddler crabs than for N. granulata because they lose the physical resource as well as the site where it was located. In contrast, N. granulata does not plug burrows during high tide and the likelihood of finding an unoccupied burrow may be much higher than in fiddler crabs. Therefore, the weak site fidelity in N. granulata may be caused by the resulting balance between the costs and benefits of guarding or defending a resource that may not be as scarce as it is for fiddler crabs. In environments in which the individuals of N. granulata are exposed to many hours of desiccation, it is common that there are almost no individuals outside the burrows and do not conglomerate in other places either, thus, in a broad sense, it can be assumed that the number of burrows are equivalent to the number of crabs. When certain zones are covered by tides a high and variable proportion of individuals leaves the burrows and has the capacity to move long distances, losing spatial contact with the original burrow. However, the total number of burrows is still equivalent to the number of crabs, so they are redistributed among the existing burrows, and the searching time and type of burrow obtained will depend on the individual relative size. For example, a male crab with a carapace width (CW) higher than 30 mm has competitive advantages of occupying a burrow with mating chamber after having abandoned its original burrow, and only at exceptional cases, we can found crabs with a smaller CW on burrows with mating chamber [32].

Our results showed that N. granulata displays different degrees of site fidelity at a geographical scale and with a variable effect of body size. In general terms, the proportion of “faithful” crabs was higher in MCH than SAO and RSJ. Within SAO and RSJ populations, smaller crabs were more “faithful” than larger ones. In this regard, many intertidal species have developed a variety of adaptations to regulate their body temperature and evaporation [63]. In the context of resource holding behaviour, the “environmentally stressful response” hypothesis predicts that individuals make behavioural decisions in order to reduce desiccation risk [64–66]. Burrows are thus essential to these crabs for avoiding adverse environmental conditions [24, 38]. A higher rate of site fidelity is thus expected in populations living under harsher climate conditions. Although the climate is less harsh in MCH than in SAO and RSJ (in terms of evaporative rate) [66, 67], its mesotidal regime results in crabs spending days without being flooded, mainly in the saltmarsh area. Under this scenario, sites with higher flooding tidal frequencies (macrotidal regimes such as SAO and RSJ) may reduce the window of exposure time to desiccation and could therefore promote lower site fidelity, thus showing that the frequency of flooding may be more important than the local evaporative rate. Indeed, the data gathered in MCH with and without a flooding strongly support the idea of the importance of tidal flooding on crab fidelity to burrows, since there are fewer “faithful” crabs during exceptional tidal events (i. e less desiccation risk during these events).

Neohelice granulata builds its burrow differently depending on the environmental characteristics (attributed mainly to different granulometry, texture and hardness of the sediment): while at some sites such as MCH and RSJ males make burrows with a mating chamber to protect the pair during mating [32, 33], at others, such as SAO, males build burrows with a widened entrance and without a mating chamber [32]. Mating chamber of MCH are maintained during all seasons independently to reproductive period, whereby in addition to the reproductive role [32], it could have another possible role, such as protection from predators, which also differed among sites (MCH have higher density of predatory avian species than SAO) [68]. In the context of resource holding behaviour, a higher rate of site fidelity is expected in populations with mating chamber because crabs assume costs of building chambers and also obtain benefits of breeding success [32]. However, the proportion of “faithful” crabs was independent of the population’s capacity to build chambers (MCH and RSJ), which may suggest that the importance to occupy a burrows with mating chambers is not as important as the environmental conditions and/or presence of predatory avian species of each saltmarsh.

Although the proportion of fidelity in SAO and RSJ always was lower than in MCH, both sites had a negative association between the probability of fidelity and crab body size. On the other hand, at MCH, there was a positive association between the probability of fidelity and body crab size for individuals under non-flooding conditions. Here, there is a case of intraspecific variation in resource holding behaviour that is dependent on body size, varying across different spatial scales (evident in SAO and RSJ vs. MCH) and flooding condition (evident in MCH). In the literature the presence of predators is reported as a factor modulating fidelity behaviour [69]. In our study case, although there are differences in the occurrence of avian predators [68] it is not clear how it may explain body-size dependent fidelity behaviour between sites. In contrast to what would be expected, sites characterized by a low density of predatory avian species [68] as SAO were those found to have body-size dependent fidelity. It is likely that other factors as different degrees of cannibalism may help to explain the relationship between site fidelity and body size. Therefore, the mobility of small individuals, at populations with high cannibalism (such as SAO [54, 70] and RSJ [Pers. Obs.]), may be less intense than those of adult due to the vulnerability to cannibalization by larger individuals [71]. Cannibalism in N. granulata is apparently density independent (since we find the lowest density of individuals where high degrees of cannibalism are reported, see Additional file 1: Fig. S3) and is rather related to proportion of organic matter content in the sediment [54, 70]. Within this context, smaller crabs could be using burrows more frequently as refuge. However, further experiments are necessary to determine whether cannibalism drives the site fidelity behaviour of smaller crabs in this population.

In the case of MCH with a positive association between the probability of fidelity and crab body size in the low tidal area, and with the exposition to a large number of predatory avian species (such as gulls Larus atlanticus, oystercatchers Haematopus palliatus, and chimangos Milvago chimango) [68], the flooding events could be the opportunity for large individuals (which are more often consumed by birds) to move about while avoiding avian predation. Similar results were reported for hermit crabs, whose dispersion and circadian rhythm are synchronised with tides, providing an advantage for dispersal and/or avoiding predators [72–75]. Thus, further experiments are needed to determine whether site fidelity behaviour (during low tide) decreases the risk of avian predation at this site.

To conclude, our study suggests that N. granulata has low burrow fidelity but the degree and dependency on body size changes according to the site. We suggest that abiotic factors such as flooding frequencies (affecting the individual desiccation risk) and biotic factors such as risk of predation-cannibalism at each site may be responsible for the differences found. In line with Cannizzo and Griffen [17], our results give a good example of how the expression of a characteristic behaviour may vary within a species depending on the environment and intrinsic characters. This probably plays an important role in structuring the spatial distribution of N. granulata along their natural range of distribution.