Symbiosis

The shells of deceased molluscs, particularly those of gastropods, provide excellent shelter from predators and are utilised by many organisms in addition to hermit crabs such as Dardanus megistos. While usually the largest occupant of the gastropod shell, hermit crabs certainly are not the sole tenant. An extensive review by Williamson and McDermott (2004) across 180 species of hermit crab found records of 550 invertebrates from 16 of the 36 animal phyla living in association with hermit crabs. This excluded algae and parasites of the hermit crabs.

A mollusc upon a mollusc! This epibiont would most likely be considered an incedental commensal, not doing any appreciable harm to the resident hermit crab. Photo: Storm Martin: Heron Island, 2012

Such a multitude of symbionts implies considerable ecological significance of hermit crabs and not surprisingly thisnhas been the focus of much research. The organisms sharing the shell of a hermit crab can be most simplistically divided into those that inhabit the lumen or internal space of the shell along with the crab and sessile organisms which attach (epibiotic) or bore (endolithic) into the shell itself. Amongst these are organisms which have significant effects upon the hermit crab, both positive and negative and those that are of negligible consequence. Further some of these symbionts are actively sought out by hermit crabs and others are obligate tenants, requiring exploitation of a hermit crab for at least some stage of their lifecycle.

Hermit crabs extend the ‘ecological life’ of their host shell which otherwise would likely become buried in sediment (Pretterebner et al. 2012). Because they provide a stable but mobile substrate, hermit crabs can be considered ecosystem engineers, globally having a substantial influence on the abundance and distribution of a variety of invertebrates (Pretterebner et al. 2012). In soft-sediment environments this is most appreciably significant as hermit crabs offer rare hard based settlement sites for a variety of organisms (Pretterebner et al. 2012). When carried by a hermit crab, a gastropod shell becomes a more attractive home than when the mollusc was alive. Even with the resident crab there is more available internal space and without continual laying down of new shell, attachment and boring becomes easier. Being mobile, hermit crabs provide other residents of the shell with additional protection from predators and access to good environmental conditions and food supply.

Animals which bore into the shell of hermit crabs are mostly represented by polychaete worms and sponges. Some species of sponge, particularly those of Cliona are considered incidental endolithic symbionts and have been suggested to negatively impact the host hermit crab by eroding and weakening the shell and thereby increasing the chances of predation. However, certain other species of sponge, while perhaps not obligate, are very common as symbionts of hermit crabs and may be associated with a substantial proportion of some hermit populations.

Polychaete worms are amongst the most represented of hermit crab symbionts and are most diverse in modes of exploitation; not only borers, some species attach to the shell externally or internally, live freely within the shell lumen and even attach to the hermit crab itself. As borers, polychaete worms have a similar negative effect as sponges, weakening the host shell. Many of those polychaetes using hermit occupied shells as attachment sites are incidental, though some are obligate. Except under heavy loads of attached polychaetes, the impact upon the hermit crab of these symbionts is typically negligible and most are therefore considered commensals, neither providing the hermit crab with any substantial benefit. Those sharing the shell lumen with the hermit crab are particularly interesting, sometimes obligate and usually with a negative impact upon the hermit crab. After sneaking past the hermit crab, a difficult task, these worms remain in the shell lumen, stealing food from the hermit crab or even feeding upon its eggs. This latter behaviour is particularly detrimental to the fitness of the hermit crab.

Various encrusting and boring symbionts are visible on this large spider conch (Lambis lambis). The resident crab is just visible retreating into the shell aperture. Highlighted are an encrusting bryozoan and the tube of a boring polychaete worm. Encrusting algae and other bryozoan colonies are also visible. Photo: Storm Martin, Heron Island, 2012

One of the most significant and well studied groups of hermit crab symbionts are the cnidarians, in particular certain anemones and various hydrozoans. These usually are beneficial to hermit crabs, their stings deterring settlement of borers and predators such as octopus. Some hermit crabs are known to actively seek and attached these cnidarians for their protective benefits, however this behaviour is not recorded from D. megistos, though it is likely some hydrozoan associations exist.

Arthropods are the other significant group commonly sharing the shell of hermit crabs, with the largest number of recorded species from the primary literature. The limited descriptions of symbionts of D. megistos are all arthropods and include copepods of the genera Paraidya, Porcellidium and Sunaristes as well as mysid shrimp of Heteromysis, an amphipod of Gitanopsis and the decapod caridean shrimp Aretopsis amabilis. All these are considered commensals, living and breeding free within the shell lumen and feeding upon food particles drawn in and missed by the filter feeding hermit crab. The mysids have further been observed (with use of glass shell replicas) to feed upon the hermit crab faeces and some amphipods have been hypothesised to feed more directly from the hermit crab body, gleaning detritus from the setae. Sharing the baler shell, Melo amphora, of largest individual D. megistos collected from Heron Island as part of this project, were a family group of Heteromysis mysid shrimp (either Heteromysis harpax or Heteromysis harpaxoides), a resident breeding pair with multiple cohorts of juvenile young (Vannini et al. 1993). The colour of these shrimp closely resembled that of D. megistos, red and white, suggesting their presence within the shell to be more than coincidence and these shrimp are indeed considered obligate commensals of several Dardanus species, including records from D. megistos at Heron Island (Bacescue and Bruce 1980 in Vannini et al. 1993).

This photo demonstrates the effectiveness of epibionts as camouflage in the field. Photo: Storm Martin, Heron Island, 2012

Aretopsis amabilis, the caridean shrimp, is a predator of smaller arthropods itself and this raises the important consideration of the gastropod shell as a small community. As well as the appreciation for the interaction between each symbiont and the hermit crab there is of course a potential interaction between each pair of these other organisms sharing the shell. This will include predation but also, more subtly, competition and exclusion in relation to food and space.

The benefits to the other organisms sharing the shell with the hermit crab are quite obvious; protection, food and a substrate which will always be carried to favourable conditions. While many of these symbionts seemingly have no impact upon the hermit crab and others may degrade the shell, steal food or even prey upon hermit crab eggs there are benefits of housing some symbionts. The protection gained from stinging cnidarians discussed above is most obvious, but additionally the numerous organisms covering the shell can provide substantial camouflage. This includes bryozoans, encrusting algae, sponges, cnidarians, polychaete worms and even other smaller molluscs.

Illustration from observation of mysid shrimp (Heteromysis sp.) found sharing lumen of a Melo amphora shell with very large Dardanus megistos. Illustration by Storm Martin, 2012	Above: Some of the family of 20 odd Heteromysis mysid shrimp sharing the shell lumen and Below: A close-up of the appearance of D. megistos, conveniently matching the colours of the obligate commensal mysids. Photos: Storm Martin, Heron Island, 2012