The unwanted guests of hermits: A global review of the diversity and natural history of hermit crab parasites

Hermit crabs (superfamily Paguroidea), by their typical nature as inhabitants of mobile, protective domiciles, are a unique source for studying symbiotic relationships. A great variety of symbionts attach, bore into or live free in the lumen of shells harboring hermit crabs, and hermit crabs themselves as hosts for a variety of parasites and potential parasites are the subject of this review. Approximately 130-140 species of the > 850 known hermit crab species are parasitized by 149 species in 9 phyla, and 27 species are hosts for 17 potential parasites in 5 phyla. Among the confirmed parasites, 30 species of parasitic barnacles (Rhizocephala) and 83 species of parasitic Isopoda are known. Species in other groups of parasites are few in number: Apicomplexa 2, Dinoflagellata 1, Microsporida 2, Ascomycota 1, Platyhelminthes 8, Acanthocephala 2, Nematoda 3, and Nematomorpha 2. Fifteen species of ectosymbiotic mites are obligate associates, but little is known of their possible parasitic tendencies. In terms of trophic strategies, the rhizocephalans, nematomorphans and two flatworm species are complete parasitic castrators and the parasitic isopods are partial parasitic castrators. The rest of the species are trophically transmitted parasites (Apicomplexa, Platyhelminthes, Acanthocephala and Nematoda) or are classified as pathogens (Apicomplexa, Dinoflagellata, Microsporida, and Ascomycota). Limited information shows that hermit crabs are first or second intermediate hosts for coccidians, cestodes, trematodes, acanthocephalans and nematodes. The importance of hermit crabs as definitive and intermediate hosts is greatly underestimated due to insufficient worldwide sampling for parasites. The ten most well-studied hermit crab host species are from European waters, the western Atlantic and the eastern Pacific. In contrast, the lower parasite diversity of the Indo-West Pacific region is presumably due to limited sampling. Hermit crabs are also known to host at least 17 species of obligate, intimate associates (not presently considered parasites), but further analyses are required to more fully clarify their symbiotic relationships. Among these potential parasites are four mesomycetozoans that are found in the digestive tract of hosts and four apostome ciliates whose reproduction is synchronized with the host's molting. Symbiotic nemerteans and octolasmid barnacles that are common associates of decapods have, surprisingly, yet to be discovered associated with hermit crabs. In total, at least ten species of hyperparasites are found infesting primary associates (mostly rhizocephalans and bopyrids) of hermit crabs. Hyperparasitism involves: 1) rhizocephalans as hosts for one described species of amoeba and four species of cryptoniscid isopods, 2) bopyrid isopods as hosts for three described species of cabiropid isopods and one rhizocephalan (Akentrogonida), and 3) a burrowing barnacle (Trypetesidae) as host for one species of hemioniscid isopod. The biology and life histories of most hermit crab parasites, with the exception of rhizocephalans and some isopods, are poorly known and the role of crabs as intermediate hosts is especially in need of study. The information presented herein on geographical distribution of host species, the prevalence of their parasites, and known host-parasite relationships should be useful for developing models that will elicit a greater understanding of hermit crab parasitism. Such information, along with morphological and molecular analyses might lead to a better understanding of the evolution of anomurans and decapods as a whole.