Invaders, natives and their enemies: distribution patterns of amphipods and their microsporidian parasites in the Ruhr Metropolis, Germany

Abstract

BackgroundThe amphipod and microsporidian diversity in freshwaters of a heterogeneous urban region in Germany was assessed. Indigenous and non-indigenous host species provide an ideal framework to test general hypotheses on potentially new host-parasite interactions, parasite spillback and spillover in recently invaded urban freshwater communities.MethodsAmphipods were sampled in 17 smaller and larger streams belonging to catchments of the four major rivers in the Ruhr Metropolis (Emscher, Lippe, Ruhr, Rhine), including sites invaded and not invaded by non-indigenous amphipods. Species were identified morphologically (hosts only) and via DNA barcoding (hosts and parasites). Prevalence was obtained by newly designed parasite-specific PCR assays.ResultsThree indigenous and five non-indigenous amphipod species were detected. Gammarus pulex was further distinguished into three clades (C, D and E) and G. fossarum more precisely identified as type B. Ten microsporidian lineages were detected, including two new isolates (designated as Microsporidium sp. nov. RR1 and RR2). All microsporidians occurred in at least two different host clades or species. Seven genetically distinct microsporidians were present in non-invaded populations, six of those were also found in invaded assemblages. Only Cucumispora dikerogammari and Dictyocoela berillonum can be unambiguously considered as non-indigenous co-introduced parasites. Both were rare and were not observed in indigenous hosts. Overall, microsporidian prevalence ranged from 50 % (in G. roeselii and G. pulex C) to 73 % (G. fossarum) in indigenous and from 10 % (Dikerogammarus villosus) to 100 % (Echinogammarus trichiatus) in non-indigenous amphipods. The most common microsporidians belonged to the Dictyocoela duebenum- /D. muelleri- complex, found in both indigenous and non-indigenous hosts. Some haplotype clades were inclusive for a certain host lineage.ConclusionsThe Ruhr Metropolis harbours a high diversity of indigenous and non-indigenous amphipod and microsporidian species, and we found indications for an exchange of parasites between indigenous and non-indigenous hosts. No introduced microsporidians were found in indigenous hosts and prevalence of indigenous parasites in non-indigenous hosts was generally low. Therefore, no indication for parasite spillover or spillback was found. We conclude that non-indigenous microsporidians constitute only a minimal threat to the native amphipod fauna. However, this might change e.g. if C. dikerogammari adapts to indigenous amphipod species or if other hosts and parasites invade.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-015-1036-6) contains supplementary material, which is available to authorized users.

Hidden diversity: parasites of stream arthropods

“…Microsporidians can be found in most groups of aquatic invertebrates and are also hyperparasites of gregarines, acanthocephalans, cestodes, trematodes and myxozoans (Morris & Freeman, ; Stentiford et al ., ). They were the most diverse and abundant group in the present study, which is in line with previous reports from aquatic organisms, such as amphipods and snails, from which high diversity and prevalence were found (Terry et al ., ; McClymont et al ., ; Krebes et al ., ; Grabner et al ., ). In the present study, some microsporidians were found only in amphipods, but were never detected in insect hosts ( Microsporidium sp.…”

“…505 and 515). The same microsporidians were previously detected in different amphipod species (Terry et al ., ; Krebes et al ., ; Grabner, Schertzinger & Sures, ; Grabner et al ., ; Weigand et al ., ), and can be considered amphipod specific. The only unique host–parasite association was found between the mayfly E. danica and the group D‐ Microsporidium .…”

“…DNA was isolated from whole invertebrates by salt precipitation according to Grabner et al (2015). Microsporidians were detected using universal microsporidian primers V1 (Zhu et al, 1993)/micro3R that amplify a part of the small subunit ribosomal RNA gene (ssu rRNA gene), as described in Weigand, Kremers & Grabner (2016).…”

Parasites, pathogens and commensals in the “low-impact” non-native amphipod host Gammarus roeselii

“…Some of the microsporidians infecting G. roeselii (Table 1) are taxa previously associated with other invasive amphipod hosts [17, 21, 22]. Some unassigned ‘ Microsporidium ’ spp .…”

Enhanced fecundity and parasite release in the first amphipod invader on the Iberian Peninsula

“…Microsporidia are intracellular, obligatory eukaryotic parasites with nonmotile walled spores, belonging to a sister clade to Fungi, Opisthosporidia, which also includes Aphelida and Cryptomycota (Corsaro et al, 2014;Haag et al, 2014;Karpov et al, 2014) and commonly infect amphipod crustaceans (Grabner et al, 2015;Terry et al, 2004). They can be transmitted vertically within the host population (transovarially, from female to offspring) or horizontally (transmission through consumption of infected tissue) causing microsporidiosis (Dunn and Rigaud, 1998;Dunn et al, 2001;Haine et al, 2004) which may be lethal Ryan and Kohler, 2010;Stentiford et al, 2013).…”