Hermit crabs and gastropods form the foundation of a complex marine ecosystem known as the gastropod shell habitat web.  Chemical signaling is known to coordinate a wide range of life processes in both crustaceans and gastropods and these signals are thought to play a role in structuring these ecosystems.  However, there has been limited investigation into the interplay between chemical communication and the distribution of organisms within their habitat.  Here, we investigate the distribution and chemical relationship between a hermit crab, Clibanarius taeniatus, and its shell-supplying gastropod, Pyrazus ebeninus, in a tidal mudflat at Cleveland Point in Redlands City, Queensland, Australia.  Our results indicate that these species are not distributed randomly throughout their environment, with hermit crabs preferring to exist near other hermit crabs, and gastropods preferring to exist near other gastropods.  Chemical signaling was also found to likely play a role in this segregated distribution, with hermit crabs preferentially moving toward a group of conspecifics in the absence of visual cues.  However, gastropods were not found to preferentially move toward conspecifics in the absence of visual cues.  Further studies should continue to examine the chemosynthetic relationships of these ecosystems and how they help shape their community structure. 

Hermit crabs and gastropods form the framework of a benthic marine ecosystem known as the gastropod shell habitat web (McLean 1983).  Gastropod shells are important resources that provide shelter and attachment substratum for a multitude of diverse marine organisms (McLean 1983).  Although unable to remove live gastropods themselves (Laidre 2011), hermit crabs play vital roles in shell acquisition and in the transportation of shells through ecosystems (McLean 1983).   The inter- and intraspecific interactions between hermit crabs and gastropods surrounding shell acquisition have been well studied.  Chemical signaling has been found to play a critical role in the mediating these hermit crab-gastropod interactions (Rittschof 1980a, b; Gherardi & Tricarico 2011).  However, the non-shell based chemical interactions within these shell-based communities have been less studied.

            Chemical communication is highly species specific and dependent upon the functional requirements of a species (Thiel & Breithaupt 2011).  Crustaceans use chemical signals for a variety of purposes, including larval settlement, parent-offspring communication, mate finding, mate choice, aggressive contests, and establishing dominance hierarchies (Thiel & Breithaupt 2011).  Hermit crabs have additionally integrated their chemical ecology with their need to locate gastropod shells (Rittschof 1980a,b; Rittschof 1990; Kratt & Rittschof 1991; Rittschof et al. 1992; Gherardi & Tricarico 2011).  The majority of research into the chemical signals and cues used within Paguroidea has been focused on crab-shell interactions (Gherardi & Tricarico 2011).  Many of these studies focus on the response of hermit crabs to odors given off by dead or dying gastropods and crushed conspecifics (Rittschof 1980a,b; Rittschof 1990; Kratt & Rittschof 1991; Rittschof et al. 1992).  In addition, other studies have explored the role of chemical cues in the ability of hermit crabs to remember and distinguish social partners (Gherardi & Atema 2005a; Gherardhi & Tricarico 2007).  However, the role chemical cues play in determining the distribution of hermit crabs throughout their environment has received far less attention.

            In 1983, Croll comprehensively outlined the importance of chemical signaling in gastropods and its associated physiology and biology.  Croll’s study found that chemoreception plays an important role in a number of gastropod functions including feeding, homing, predator avoidance, and a range of social behaviors (Croll 1983).  Since then, the chemical ecology of gastropods within shell-based habitat webs has received far less attention in literature, especially when compared with hermit crabs.  The research that has been published in this area has focused primarily on predator avoidance through both predator derived chemical cues and conspecific alarms (Jacobsen & Stabell 2004; Keppel & Scrosati 2004; Mach & Bourdeau 2011), interactions between native and non-native species (Raw et al. 2013), and trail following (Ng et al. 2013).  However, similarly to hermit crabs, the interaction between gastropod chemical ecology and their distribution throughout their habitat is yet to be explored.

            Understanding the role chemical cues play is crucial to gaining a greater understanding of the factors that shape marine ecosystems and their community structure (Hay 2009).  Although chemical signaling has been studied in gastropods and hermit crabs, the impact of chemically mediated behaviour on the ecosystem and community structure of shell-based habitats has been unexplored.  To date most studies on chemoreception in hermit crabs and gastropods have focused on their behavioural response to specified chemical cues associated with particular events (e.g., odours given off by conspecific hemolymph, dead gastropods, non-native species, predators, etc.).  However, understanding the chemically mediated behaviour of marine organisms under neutral conditions is just as important as understanding reactions to specified chemical cues.  Chemical cues are pervasive throughout all marine systems at every scale (Hay 2009) and in order to understand how these cues impact the distribution of organisms, we must know more about the intrinsic chemosynthetic relationships between organisms.   

This study will investigate the involvement of chemical signaling in the distribution of hermit crabs and their shell-supplying gastropod throughout a tidal ecosystem.  This will be addressed through laboratory experiments and an observational study conducted on the Cleveland Point mudflat in Redlands City, Queensland, Australia using yellow-striped hermit crabs (Clibanarius taeniatus) and Hercules club mud whelks (Pyrazus ebeninus).  As a preliminary study to assess whether P. ebeninus and C. taeniatus specimens exist closer to individuals of their own species in the field, we tested the hypothesis that: (1) the identity composition of a specimen’s five nearest neighbours in the field would vary dependent on whether that specimen was P. ebeninus or C. taeniatus.  The results of this preliminary study provided the rationale to investigate whether chemical cues were involved in determining these species’ segregated distributions.  To address this question we also asked the hypotheses that: (2) P. ebeninus would prefer to move towards members of its own species and away from C. taeniatus in the absence of visual cues, and (3) that C. taeniatus would prefer to move toward members of its own species and away from P. ebeninus in the absence of visual cues.

Although both species existed across the entire mudflat, specimens did appear to aggregate in areas with certain environmental conditions.   The whelks were observed to exist at the highest densities in areas of soft, muddy sediment, that were not inhabited by fiddler crabs, on the edges of tidal pools (Figure 6).   On the other hand, the hermit crabs seemed to exist at the highest densities in submerged seagrass meadows within the mudflat, where they appeared to form clear aggregations (Figures 7 & 8).   These observations suggest that resource partitioning may also play a role in determining the distributions of these two species.  However, because both specimens did not exclusively occur in these regions and were found in the majority microhabitats across the mudflat, there are perhaps other factors impacting the distributions of these organisms within their environment.
            The results of the observational field study show that the neighbour compositions of the two species did indeed vary, with P. ebeninus specimens being surrounded primarily by other whelks and C. taeniatus specimens being surrounded primarily by other hermit crabs.  Because the nearest neighbour composition varied based on species, it can be inferred that these species are not distributed randomly throughout their environment.  The findings also support the assumption that hermit crabs prefer to exist near hermit crabs and whelks prefer to exist near whelks.  This provided both a rationale performing the lab experiment and an expectation that hermit crabs specimens should prefer to move toward other hermit crabs and whelk specimens should prefer to move toward other whelks.
The results of the lab experiment indicate that the hermit crabs were indeed able to sense chemical cues in the water and had a preference to move toward conspecifics rather than whelks.  This indicated that they are likely playing a role in determining the distribution of these organisms in their ecosystem.  However, we are unable to determine whether these hermit crabs were attracted to a chemical signal produced by the group of conspecifics or repelled by a signal produced by the group of whelks.  Based on the results of Gherardi & Atema (2005b), it is unlikely that live chemical cues given off by live gastropods are repelling the hermit crabs.  In Gherardi & Atema’s study hermit crabs were found to be insensitive to odours given off by live snails (Gherardi & Atema 2005b).  On the other hand, the results of the gastropod trials indicate that the snails had no preference to move toward either a group of conspecifics or a group of hermit crabs.  However, this is not necessarily an indication that the gastropods were unable to detect chemical signals or that they do not respond to them.  These inconclusive results simply indicate that the whelks did not have a preference to move toward a group of conspecifics under this particular set of experimental conditions.  It is possible that the container used in the experiment was small enough that the specimens felt close enough to the whelks on when exiting either side of the decision chamber.  It is also possible that the non-random distribution of whelks in the field is the result of a chemical cue from an organism not used in this experiment.  Resource partitioning is also thought to play a role in these species’ non-random distributions, so future experiments would be needed to assess its relative contribution and how it relates to chemical communication.
Due to time constraints, control experiments could not be conducted, making the results of this experiment a bit unreliable.  Future studies could be improved by including a series of three control experiments with: (1) no organisms in either enclosure, (2) hermit crabs in one enclosure and no organisms in the other, and (3) gastropods in one enclosure and no organisms in the other.   This would allow us to ensure that the experimental set up was not biased toward either side of the container and also determine whether the organisms were responding to inter- or intraspecific chemical signals.
The overwhelming majority of studies previously conducted on the chemical ecology of gastropods and hermit crabs within gastropod shell-based communities have focused on shell acquisition (Rittschof 1980a,b; Rittschof 1990; Kratt & Rittschof 1991; Orihuela et al. 1992; Rittschof et al. 1992; ch15 textbook; Tricarico et al. 2011; De Souza et al. 2016).  It is hard to make comparisons between our study and the conclusions drawn in these previous studies because the majority of them have simulated particular events to assess the response of their organism (i.e. ones that would signal that availability of a gastropod shell).  Also, the studies that have investigated the response of hermit crabs to live conspecifics and gastropods gauged their response through shell investigatory behaviour (Tricarico et al 2011).  There is also little information in literature to compare the gastropod experimental results to as the majority of studies have looked at gastropod response to predator-related chemical stimuli, and C. taeniatus is not known to predate upon P. ebeninus (Jacobsen & Stabell 2004; Keppel & Scrosati 2004; Mach & Bourdeau 2011).
            Given the broad scope of life processes thought to be coordinated by chemical communication in both gastropods and crustaceans (Kohn 1961; Croll 1983; Thiel & Breithaupt 2011), it is very likely that chemical cues do play a role in determining the distribution of these organisms across their habitat.   We know chemical cues are being utilized by these organisms because of the extensive research exploring their role in mitigating the movement of shells through these habitats (Rittschof 1980a,b; Rittschof 1990; Kratt & Rittschof 1991; Orihuela et al. 1992; Rittschof et al. 1992; Gherardhi & Tricarico 2011; Tricarico et al. 2011; De Souza et al. 2016).  Because chemical communication is subject to such rapid evolutionary change (Thiel & Breithaupt 2011), it is possible that these shell-based habitat webs have an extensive and complex chemical ecology that is involved in far more than shell exchange alone.  It is important to understand the intrinsic chemical relationships between these organisms and the role these relationships play in why these species are distributed the way in which they are.  Future research should move toward investigating the extent to which chemical communication is utilized in these ecosystems and the processes in which it is involved.  

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