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

Abstract

Symbionts are a fundamental component of biological systems, and their survival is highly dependent on transmission and host movement. Ectosymbionts of amphibious animals face the added challenge of having to survive dramatic environmental changes as their hosts cross ecosystem boundaries. Within freshwaters, crayfish are amongst the most widespread invasive species that readily disperse overland and are host to a wide range of ectosymbionts. Relatively little is known about the transmission of these ectosymbionts, including their ability to survive overland host migration. Here, we assessed terrestrial emigration and both inter-and intra-specific transmissions of Xironogiton victoriensis, a nonnative branchiobdellidan (Annelida: Clitellata) recently found on invasive signal crayfish (Pacifastacus leniusculus) in the UK. These branchiobdellidans tolerated desiccation and did not alter host terrestrial behaviour. Transmission was rapid between natural signal and novel virile (Orconectes cf. virilis) crayfish hosts, with host interactions facilitating transmission.Thus, branchiobdellidans can disperse via amphibious host behaviour and readily infect novel hosts. These traits facilitate symbionts' survival and provide access to additional dispersal pathways that are likely to aid transmission.

<p class="HeadingRunIn"><strong>North American Branchiobdellida (Annelida: Clitellata) or Crayfish Worms in France: the most diverse distribution of these exotic ectosymbionts in Europe</strong></p>

“…It is most probable crayfish were present, but they eluded capture during the collection period. Although free-living branchiobdellidans have been recorded in similar situations (Holt 1973;Timm 1991) and experimentally by Hunt et al (2018), other extensive examinations of substrate samples have not found these worms (James et al 2017, Gelder unpub. data).…”

“…Whether this reflected a host preference is difficult to say. However, it should be remembered that crayfish can travel overland from one freshwater sources to another, e.g., ponds, streams, seeps, and as demonstrated experimentally (Hunt et al 2018) are capable of carrying viable branchiobdellidans with them.…”

“…Therefore, endemic associations once restricted to a region can no longer be assumed, as uncontrolled and new crayfish translocations continue to occur. The usual method of branchiobdellidan transfer from one host to another is during direct contact (Hunt et al 2018). Alternatively, branchiobdellidans will leave the host following molting, bodily damage and death, to live on the substratum until another crayfish comes in contact with them, whether endemic or acceptable exotic.…”

The interplay of nested biotic interactions and the abiotic environment regulates populations of a hypersymbiont

“…When attached to their hosts, adult ciliates of the genus Lagenophrys have the ability to seal their bodies hermetically within their lorica to avoid desiccation when they leave water (Clamp, ). The amphibious behaviour of crayfish offers opportunities for their aquatic symbionts to disperse among isolated ponds, or different riverine systems (Hunt et al, ). Moreover, the introduction and spread of the crayfish P. clarkii in the Iberian Peninsula was driven by human‐mediated translocations (Mestre et al, ).…”

“…Second, sessile adults passively disperse among crayfish within a locality via dispersal of the symbiotic ostracods (Mestre, Castillo‐Escrivà, Rueda, Monrós, & Mesquita‐Joanes, ). Third, crayfish dispersing among localities (Hunt, Thomas, James, & Cable, ; Mestre et al, ) likely disseminate ciliates carried by symbiotic ostracods, a dispersal mechanism called hyperphoresy (Sabagh, Dias, Branco, & Rocha, ).…”