Pathogens of Dikerogammarus haemobaphes regulate host activity and survival, but also threaten native amphipod populations in the UK

Abstract

Dikerogammarus haemobaphes is a non-native amphipod in UK freshwaters. Studies have identified this species as a low-impact invader in the UK, relative to its cousin Dikero gammarus villosus. It has been suggested that regulation by symbionts (such as Microsporidia) could explain this difference in impact. The effect of parasitism on D. haemobaphes is largely unknown. This was explored herein using 2 behavioural assays measuring activity and aggregation. First, D. haemobaphes were screened histologically post-assay, identifying 2 novel viruses (D. haemo baphes bi-facies-like virus [DhbflV], D. haemobaphes bacilliform virus [DhBV]), Cucumispora ornata (Micro sporidia), Apicomplexa, and Digenea, which could alter host behaviour. DhBV infection burden increased host activity, and C. ornata infection reduced host activity. Second, native invertebrates were collected from the invasion site at Carlton Brook, UK, and tested for the presence of C. ornata. PCR screening identified that Gammarus pulex and other native invertebrates were positive for C. ornata. The host range of this parasite, and its impact on host survival, was additionally explored using D. haemobaphes, D. villosus, and G. pulex in a laboratory trial. D. haemo baphes and G. pulex became infected by C. ornata, which also lowered survival rate. D. villosus did not become infected. A PCR protocol for DhbflV was also applied to D. haemobaphes after the survival trial, associating this virus with decreased host survival. In conclusion, D. haemobaphes has a complex relationship with parasites in the UK environment. C. ornata likely regulates populations by decreasing host survival and activity, but despite this benefit, the parasite threatens susceptible native wildlife.

The mitochondrial genome of UK (non-native) Dikerogammarus haemobaphes (Amphipoda: Gammaridae) informs upon Dikerogammarus evolution, invasions and associated microparasites

“…The demon shrimp, Dikerogammarus haemobaphes (Eichwald 1841), is a non-native freshwater amphipod in the UK that exerts low levels of ecological damage and inter-species competition (Bovy et al, 2015). The species hosts multiple mortality-inducing and behaviour-altering pathogens that have been carried alongside the invasion into the UK (Bojko et al, 2018a). Infection with the microsporidian pathogen Cucumispora ornata Bojko, Dunn, Stebbing, Ross, Kerr, Stentiford 2015 was noted to reduce activity in heavily infected hosts and was associated with mortality in both D. haemobaphes and non-target Gammarus pulex (L.), which also have the infection in wild populations (Bojko et al, 2018a).…”

“…The species hosts multiple mortality-inducing and behaviour-altering pathogens that have been carried alongside the invasion into the UK (Bojko et al, 2018a). Infection with the microsporidian pathogen Cucumispora ornata Bojko, Dunn, Stebbing, Ross, Kerr, Stentiford 2015 was noted to reduce activity in heavily infected hosts and was associated with mortality in both D. haemobaphes and non-target Gammarus pulex (L.), which also have the infection in wild populations (Bojko et al, 2018a). 'Dikerogammarus haemobaphes bi-facies-like Virus' (DhbflV), was also identified as a mortality-inducing virus at low prevalence within the D. haemobaphes population in the UK (Bojko et al, 2018a).…”

“…Infection with the microsporidian pathogen Cucumispora ornata Bojko, Dunn, Stebbing, Ross, Kerr, Stentiford 2015 was noted to reduce activity in heavily infected hosts and was associated with mortality in both D. haemobaphes and non-target Gammarus pulex (L.), which also have the infection in wild populations (Bojko et al, 2018a). 'Dikerogammarus haemobaphes bi-facies-like Virus' (DhbflV), was also identified as a mortality-inducing virus at low prevalence within the D. haemobaphes population in the UK (Bojko et al, 2018a). Finally, a likely novel member of the Nudiviridae, 'Dikerogammarus haemobaphes Bacilliform Virus' (DhBV) was found to increase the activity of its host and potentially alter the rate of invasion spread (Bojko et al, 2018a).…”

“…'Dikerogammarus haemobaphes bi-facies-like Virus' (DhbflV), was also identified as a mortality-inducing virus at low prevalence within the D. haemobaphes population in the UK (Bojko et al, 2018a). Finally, a likely novel member of the Nudiviridae, 'Dikerogammarus haemobaphes Bacilliform Virus' (DhBV) was found to increase the activity of its host and potentially alter the rate of invasion spread (Bojko et al, 2018a).…”

A New Family of DNA Viruses Causing Disease in Crustaceans from Diverse Aquatic Biomes

“…Several potential NCLDVs have been identified from crustacean hosts, but these do not appear to replicate in the cytoplasm (as generally expected of NCLDVs) and remain to be studied systematically (4)(5)(6)(7). These viruses develop within the nucleus of crustacean host hemocytes and hemopoietic tissues, resulting in anemia and subsequent death.…”