Reduced aggression and foraging efficiency of invasive signal crayfish (Pacifastacus leniusculus) infested with non-native branchiobdellidans (Annelida: Clitellata)

Abstract

BackgroundBiological invasions are a principal threat to global biodiversity and identifying the determinants of non-native species’ success is a conservation priority. Through their ability to regulate host populations, parasites are increasingly considered as important in determining the outcome of species’ invasions. Here, we present novel evidence that the common crayfish ecto-symbiont, Xironogiton victoriensis (Annelida: Clitellata) can affect the behaviour of a widespread and ecologically important invader, the signal crayfish (Pacifastacus leniusculus).MethodsTo assess the signal crayfish–X. victoriensis relationship naïve crayfish were infested with an intensity of worms typically observed under natural conditions. Over a 10-week period the growth rate and survivorship of these animals was monitored and compared to those of uninfested counterparts. Complementary dyadic competition and foraging experiments were run to assess the behaviour of infested compared to uninfested animals. These data were analysed using General Linear Models and Generalized Linear Mixed Models.ResultsWhilst X. victoriensis did not affect the growth rate or survivorship of signal crayfish under laboratory conditions, infested animals were significantly less aggressive and poorer foragers than uninfested individuals.ConclusionsThrough reducing aggression and foraging efficiency, infestation with X. victoriensis may disrupt the social structure, and potentially growth rate and/or dispersal of afflicted crayfish populations, with potential effects on their invasion dynamics. This is important given the widespread invasive range of crayfish and their functional roles as ecosystem engineers and keystone species.

Assessing the invasion potential of non-native branchiobdellidans: experimental studies of survival, reproduction and competition

“…Considering its ability to reproduce in vitro, C. aff. okadai, is likely a facultative symbiont, whereas X. victoriensis, considering its dependency on the host to reproduce and the detrimental effect it is known to have on host behaviour (James et al, 2015b), is an obligate symbiont that may be parasitic. Therefore, whilst both species have established in the UK and are predicted to spread with the dispersal of signal crayfish, X. victoriensis may have greater potential to influence ecosystem structure and function.…”

“…If niche overlap between these branchiobdellidans was forced, for example by removal of signal crayfish from the River Gavenny for control (reducing the number of available hosts), intraguild predation would likely become more important. Ultimately, this could impact the survival of competitively subordinate X. victoriensis, which are known to reduce the aggression and foraging success of infected crayfish (James et al, 2015b).…”

“…Signal crayfish are widespread across the UK , and have altered the structure and function of recipient ecosystems throughout their non-native range (James et al, 2015c). Under laboratory conditions, X. victoriensis reduces aggression and foraging efficiency of signal crayfish (James et al, 2015b), which may alter host invasion dynamics in the field. Given the high frequency of co-infection between C. aff.…”

The redclaw crayfish: A prominent aquaculture species with invasive potential in tropical and subtropical biodiversity hotspots

“…These include local crabs rather than shrimps with more developed grooming behaviour (Du Preez & Smit 2013;Tavakol et al 2016;Douthwaite et al 2018). Recent research suggested altered behaviour of competing branchiobdellids (James et al 2017) and their translocated host (James et al 2015). These previously overlooked consequences (Vedia et al 2015) can be thus expected also among translocated temnocephalids and their hosts.…”

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

“…This location may facilitate transmission as crayfish often lock chelae during aggressive interactions, but it could also promote desiccation during terrestrial host movements. Although branchiobdellidans are generally considered commensals, X. victoriensis reduces crayfish aggression and foraging efficiency, which could alter signal crayfish invasion success (James et al, 2015c). Here, we tested whether these aquatic ectosymbionts can tolerate amphibious host behaviour, which in turn could affect symbiont dispersal with potential consequences for host invasion dynamics.…”