Our records of shore crabs (C. maenas) infested with adult females of P. maenadis at two locations in the Wadden Sea close a distribution gap of this entoniscid species between previous southern observations in Portugal and France and northern occurrences from Denmark and Sweden. It is the first record for the Wadden Sea region and the second record for the North Sea as a whole aside from a specimen from the Firth of Forth in Scotland which stems from a private collection from approximately 1920/1930 which was integrated into the collection of the Natural History Museum London in 1958 (Natural History Museum 2019). Since then, there have been several parasitological studies on shore crabs (C. maenas) in the North Sea area, none of which observed P. maenadis (Goudswaard 1985; Stentiford and Feist 2005; Thieltges et al. 2008; Blakeslee et al. 2009; Zetlmeisl et al. 2011; Goedknegt et al. 2017; Bojko et al. 2018). This indicates that the parasite is relatively rare and has a very patchy distribution on a regional scale. This also seems to be true on a local scale as we only found P. maenadis at one of the two locations sampled on each island; however, we acknowledge that the sample size in our survey was relatively small. At locations where P. maenadis is generally present, it is not very common in crab hosts and prevalence is usually well below 10% in the adult crab population as indicated from our literature survey. However, in some cases, higher prevalence has been observed (Table 1) and, in particular, our observation of a prevalence of 45% in adult crabs sampled in November 2018 at Texel in the southern Wadden Sea seems to be unique. The prevalence (50%) at the southern location of Sylt needs to be interpreted with caution, since only two adult individuals were investigated for the parasite infestation.
Why the occurrence of P. maenadis is so patchy and why prevalence differs among locations is not known and we can only offer speculation. Some of the patterns observed may result from the life cycle of the parasite which involves two sequential hosts (for more details see Veillet 1945, Williams and Boyko 2012). From the eggs of P. maenadis, epicaridium larval stages hatch and infest calanoid copepods (intermediate host). The larvae settle on the outer body wall of the copepods and metamorphose into a microniscus stage that lives ectoparasitically and feeds on the host’s haemolymph. At some point, the microniscus larvae abandon the copepod host and turn into free-living cryptoniscus larvae that intrude into the abdominal cavity of shore crabs (definitive host). Here females metamorphose into a sack-like structure (Fig. 2b) and grow by feeding on the hemolymph in the hemocoel to about 4 cm length while males turn into a sexually mature form of only 1–3 mm in length. This life cycle makes it necessary that all suitable hosts are locally present and that males and females occur together in infected crabs and it seems reasonable to assume that this results in the patchy distribution and the low prevalence generally observed in P. maenadis. The observed drop in prevalence from November 2018 to April 2019 at Texel could relate to seasonal patterns of infestation but whether such patterns exist is difficult to tell as only observations from summer are available from the literature (see Online Resource 1).
Alternatively, the drop in infestation levels between our sampling events may indicate a negative effect of P. maenadis on crab fitness. As adult parasites feed on their hosts’ haemolymph they are likely to have consequences for the hosts’ energy budgets. Such an energy burden is generally observed in hosts of epicaridean parasites and assumed to ultimately lead to castration of the host (O’Brien and Van Wyk 1985). The energy drain caused by the parasites may be particularly deleterious in the winter months when food is scarce and may elevate mortality of infected crabs, leading to the observed drop in prevalence in spring. However, experimental studies would be needed to investigate whether this speculative mechanism actually exists. In addition to potential energetic effects, infestations with P. maenadis may also lead to morphological changes in the form of feminisation of male crabs (i.e. broader pleon, slender claws, bulging carapace; Rasmussen 1973). This was also observed in our samples from the Wadden Sea (Fig. 2c). Whether there are also behavioural and distributional changes associated with infestations such as the ones observed in infestations with the rhizocephalan Sacculina carcini Thompson, 1836, which makes male and female crabs behave like egg-bearing females, moving into deeper waters (Waser et al. 2016), is unclear and remains to be studied. We hope that the results of our sampling of P. maenadis in the Wadden Sea and the additional literature review on its European distribution will stimulate future research into the occurrence of this intriguing parasite species as well as on the impacts of parasite infestations on host populations and community ecology in general, because the role of parasitism in shaping communities may be of equal importance as other biotic factors such as predation and competition (Thieltges et al. 2018).