An investigation of microparasites and microbes in four decapod crustaceans

Abstract

Crustaceans are valuable components of their ecosystems and support fisheries of economic value. As these fisheries continue to grow worldwide, and particularly for wild decapod crustaceans, it is important to monitor the factors affecting their health in order to ensure appropriate sustainable management measures and to protect crustacean populations from declines. Parasites are one challenge facing crustacean populations which can affect the behaviour, and physiology of their crustacean hosts, as well as causing high rates of mortality in some cases. The research carried out here aimed to investigate patterns of microparasite infections in four commercial decapod crustacean species; velvet crab (Necora puber), edible crab (Cancer pagurus), spider crab (Maja squinado), and European lobster (Homarus gammarus). Firstly, we carried out a two-year sampling program of velvet crab (Necora puber) in Galway Bay to identify microparasite prevalence and variability in infection, with particular focus on the recently discovered paramyxid Paramarteilia canceri. We found a high prevalence of the parasite overall with both seasonal and annual variation. We examined different host tissues and organs to better understand the biology of infections. Finally, we provide the first genetic confirmation of the parasite in the gonad and eggs of a berried female, suggesting vertical transmission as a possible transmission route for P. canceri, and highlighting the need for further investigation into the lifecycle of this parasite. The hepatopancreas was identified as one of the organs often infected by the parasite and therefore to further examine the potential impacts of parasite infection, we investigated the hepatopancreas microbiome of velvet crab. Through the use of next generation sequencing of the 16S rRNA gene, we provide the first description of the hepatopancreas microbiome and we analysed whether infection by P. canceri affected variation in the microbiome. We found no significant variation in the microbiome due to parasite presence but we did find a difference between samples collected at two different sampling points. We also identified a core microbiome present in the hepatopancreas which will provide a baseline for future studies on velvet crab microbiomes and health investigations. To more broadly investigate microparasite infections in decapod crustaceans, we screened for three important parasite groups; microsporidians, Hematodinium spp, and P. canceri in velvet, spider, and edible crabs and in lobster. The paramyxid P. canceri was identified in all three crab species and we provide novel genetic sequences for each. Microsporidians were found only in velvet crab and we identified two different species, one Ameson sp., a genus known to negatively impact the muscle of crabs, and one unidentified species which will need further study. Going beyond microparasites only, we carried out a systematic review of the literature to gain an overview of the mortality impact of parasites on crustaceans. We found that increased mortality in crustacean hosts infected with parasites was reported from more than half of the records we analysed. Records were from a range of hosts, but most were from amphipods and decapods, which both had a high percentage of records reporting an increase in mortality with parasite infection. Records were also from a range of parasites, with most records were from protists, oomycetes, and trematodes, for which records reporting an increase in mortality ranged from <50% to >80%. Overall, the results of this research provide valuable information on microparasite patterns of infection and interactions with several crustacean hosts, novel insights into the hepatopancreas microbiome of velvet crab, and an overview of the literature on the mortality effects of parasites in crustaceans. We recommend that parasites in crustaceans continue to be investigated in scientific studies and for regular monitoring of crustaceans, particularly in fisheries, there is a need to understand the impacts of parasites and quantify parasite-induced mortality and include this in stock assessments. Further work is needed to assess parasite impacts at a population level and how this interacts with other ecosystem and human elements, providing opportunities for sustainable management of crustacean populations.