Ontogenetic shifts in a freshwater cleaning symbiosis: consequences for hosts and their symbionts

Abstract

Animal fitness is influenced by diverse assemblages of internal and external symbionts. These assemblages often change throughout host ontogeny, but the mechanisms that underlie these changes and their consequences for host fitness are seldom revealed. Here we examine a cleaning symbiosis between crayfish and an assemblage of ectosymbiotic branchiobdellidan worms to uncover what mechanisms drive changes in symbiont composition during host ontogeny and the consequences of these changes for both the host and symbionts. In surveys of a North Carolina river, the dominant worm species shifted from Cambarincola philadelphicus to Cambarincola ingens as crayfish (Cambarus bartonii) increased in size. We demonstrate that this shift is a function of host regulation by small crayfish and exclusion by a dominant symbiont on large crayfish. In a controlled lab experiment, small crayfish often removed their symbionts but C. ingens was removed at a higher rate than C. philadelphicus. In contrast, C. ingens had higher survivorship and reproduction than C. philadelphicus on large crayfish. We also measured the effect of each worm species on crayfish growth through ontogeny; neither worm species had an effect on small crayfish but both species had similar positive effects on the growth of large crayfish relative to controls. Evidence from another experiment suggested that intraguild predation by C. ingens caused a decline in C. philadelphicus on large crayfish. We have shown that shifts in partner fitness are a function of host size and that these shifts can involve the succession of symbionts. Further, our results suggest that changes in the outcome of symbioses can remain robust throughout host ontogeny despite interactive mechanisms that lead to shifts in symbiont community structure.

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

“…Intraguild predation has previously been observed in congeneric branchiobdellidans, with C. vitreus being consumed by C. chirocephalus, which has a larger jaw size (Gale and Proctor, 2011). Intraguild predation is an important component of crayfish symbioses (Thomas et al, 2016), however to date the presence of C. aff. okadai has not prevented the establishment of X. victoriensis in the River Gavenny, most likely because they occupy separate host micro-habitats (James et al, 2015a).…”

Mutualism or parasitism: Partner abundance affects host fitness in a fish reproductive interaction

“…Although ecologists broadly recognise that mutualism is ubiquitous in nature (Bronstein, 1994a;Herre, Knowlton, Mueller, & Rehner, 1999;Sachs, Mueller, Wilcox, & Bull, 2004;Sachs & Simms, 2006;Stachowicz, 2001), it has until recently been largely overlooked in freshwater systems (Holomuzki et al, 2010). In addition to a few other interaction types (worm/crayfish cleaning symbiosis; Brown et al, 2002Brown et al, , 2012Lee et al, 2009;Skelton et al, 2013;Thomas, Creed, Skelton, & Brown, 2016; frugivorous fish seed dispersal- Correa et al, 2015;Horn et al, 2011), nest associative spawning fishes provide an excellent model system for understanding mutualisms and context dependency in freshwater ecosystems. Mutually beneficial nest associations have been documented previously in systems of other nest building taxa (Goff, 1984;Johnston, 1994b;Wisenden & Keenleyside, 1992), and more recently with Nocomis hosts (Peoples & Frimpong, 2013).…”

Positive biotic interactions in freshwaters: A review and research directive

“…This grooming behaviour is also affected by host ontogeny, with host age and size influencing worm removal (Skelton, Creed, & Brown, 2014, 2015. Because young crayfish frequently moult, which relieves their gills of fouled cuticles, they do not benefit from hosting worms and thus remove them (Thomas, Creed, Skelton, & Brown, 2016). Older crayfish moult less, and allow worms to colonise and engage in a mutualism (Skelton et al, 2014;Skelton, Doak, Leonard, Creed, & Brown, 2016b).…”