An alien ectosymbiotic branchiobdellidan (Annelida: Clitellata) adopting exotic crayfish: a biological co-invasion with unpredictable consequences

Abstract

Invasive alien species present a global threat to biodiversity, particularly where pathogens and symbionts are involved. Branchiobdellidans are clitellate annelids with an obligate ectosymbiotic association primarily on astacoidean crayfish. There are several examples of branchiobdellidan species adopting a geographically exotic host where endemic and exotic crayfishes cohabit the same water body. The first records of a western North American branchiobdellidan, Xironogiton victoriensis, adopting the eastern North American crayfish, Procambarus clarkii, in 2 river basins in Spain provide further evidence of the ectosymbionts' tolerance to adopt an exotic host. Given worldwide translocations of these and other commercial crayfish species, limnologists and agency managers need to be alert for further introductions of X. victoriensis and other branchiobdellidans. Impacts of these exotic ectosymbionts on habitat and biota at a new location are unknown, as are their consequences on native biodiversity.

Transmission and terrestrial dispersal of non-native ectosymbionts on invasive crayfish

“…This supports previous reports indicating that whilst some branchiobdellidan species exhibit host preferences (Brown & Creed, 2004), most crayfish species are acceptable hosts (alongside certain crabs and shrimps; Gelder & Messick, 2006;Govedich et al, 2009;Niwa et al, 2014). X. victoriensis has been reported on invasive red swamp crayfish populations in Spain, likely due to cohabitation with infected signal crayfish (Vedia et al, 2014). Red swamp and virile crayfish are present in the UK together with five other non-native and one native crayfish species .…”

“…Their relationship with crayfish can vary across the symbiosis continuum (Lee et al, 2009;Brown et al, 2012;Thomas et al, 2016) and as such, they have the capacity to affect host invasion dynamics. Branchiobdellidans possess several characteristics associated with successful invaders, including a direct life cycle (Young, 1966;Creed et al, 2015) and broad host range (Goodnight, 1940; although host preference does occur in some species, see Brown & Creed, 2004), which has led to invading branchiobdellidan species spreading to novel hosts (Sobecka et al, 2011;Vedia et al, 2014). Considering the number of non-native crayfish introductions into Europe, reports of introduced branchiobdellidans are relatively few.…”

Annelid symbiont assemblage and European stone crayfish − a deterministic relationship with implications for conservation management

“…As previously reported, human-mediated translocations of crayfishes imply not only risks due to the potential invasiveness of the crustaceans themselves (Gherardi, 2007), but also due to the introduction of exotic epibiont species into new habitats (Vedia et al, 2015;James et al, 2017). Likewise, evidence was found here that B. balcanica does not occur naturally in the European Rhine catchment, and thus the introduction of this species should be avoided.…”

“…In this regard, human-mediated introductions of non-indigenous crayfish species into European inland waters are considered to be a major threat for both the native crayfish (Holdich et al, 2010) and the crayfishbranchiobdellidan relationship. As non-indigenous crayfishes carry exotic Branchiobdellida species, there is not only a competitive interaction between the crustacean invaders and the native crayfishes, but potentially negative effects for the mutualistic crayfish-branchiobdellidan relationship due to the introduction of new crayfish worm species (Vedia et al, 2015;James et al, 2017).…”

Preliminary data on the distribution, morphology and genetics of white-clawed crayfish and on their ectosymbionts in Lunigiana (Tuscany, Italy)

“…Nevertheless, the occurrence of Branchiobdellida in only one of the two streams deserves some attention. Branchiobdellidans are obligate ectosymbionts of crayfish and, depending on different environmental conditions, they can act as commensals, mutualists or parasites (Scalici et al, 2010a;Brown et al, 2012;DeWitt et al, 2013;Skelton et al, 2013;Vedia et al, 2014;Skelton et al, 2016;Vedia et al, 2016). Some species of branchiobdellidans can positively influence their hosts' body size and mass (Keller, 1992;Brown et al, 2002;DeWitt et al, 2013;Vedia et al, 2016).…”