Slipping past the doorman: Host control shapes succession-like patterns in ectosymbiont assemblages
Mutualisms are best viewed as reciprocal exploitations, often with co-evolved systems of controls that allow species to exploit each other without themselves being overexploited. Changes in the costs and benefits of symbiosis that occur with ontogeny can add another layer of complexity to such interactions. In the cleaning symbiosis between crayfish and ectosymbiotic crayfish worms (Branchiobdellida), worms clean epibiotic material from their host and, as a result can increase crayfish growth and survivorship. However, worms may also act as parasites by feeding on host tissues, especially at high worm densities. Recent work suggests that crayfish limit parasitism through restrained removal and consumption of their worms. Moreover, this control is adjusted throughout crayfish ontogeny to reflect changes in the costs and benefits of symbiosis; younger crayfish are less tolerant of worms than older crayfish. Previous work investigating host control has only considered single crayfish/worm species pairs. But crayfish often harbor multi-species assemblages of worms and the diversity of worms which share limited space and resources on a common host suggests multiple successful co-evolved strategies for symbiosis. We combined field observations with experimentation to explore varying host control over multiple co-occurring worm species and relate differences to species-specific worm characteristics.
At multiple sampling locations, we found consistent species-specific patterns in worm prevalence and relative abundance through crayfish ontogeny. Some species showed marked increases with increasing host size (late arrivers), whereas others showed no relationship or even declined with host size (early arrivers). These contrasting patterns resulted in compositional changes of worm assemblages reminiscent of succession. In general, species with similar attachment site preferences displayed similar patterns in prevalence and relative abundance through host ontogeny. A series of manipulative experiments designed to assess host control over multiple worm species demonstrated that late arrivers were likely to be removed from small hosts, but more likely to persist on larger hosts. Conversely, the persistence of early arrivers was unaffected by host size or host control. This suggests that the succession-like patterns observed in worm assemblages are largely driven by varying effects of host control on different worm species. Our work shows that controls that change with symbiont ontogeny can interact with the specific characteristics of multiple partners to shape patterns in symbiont assemblages and perhaps increase symbiont diversity.