license: Copyright © Cambridge University Press 2013 0000-0001-7279-715

Changes in host phenotype are often attributed to manipulation that enables parasites to complete trophic transmission cycles. We characterized changes in host phenotype in a colonial host–endoparasite system that lacks trophic transmission (the freshwater bryozoan Fredericella sultana and myxozoan parasite Tetracapsuloides bryosalmonae). We show that parasitism exerts opposing phenotypic effects at the colony and module levels. Thus, overt infection (the development of infectious spores in the host body cavity) was linked to a reduction in colony size and growth rate, while colony modules exhibited a form of gigantism. Larger modules may support larger parasite sacs and increase metabolite availability to the parasite. Host metabolic rates were lower in overtly infected relative to uninfected hosts that were not investing in propagule production. This suggests a role for direct resource competition and active parasite manipulation (castration) in driving the expression of the infected phenotype. The malformed offspring (statoblasts) of infected colonies had greatly reduced hatching success. Coupled with the severe reduction in statoblast production this suggests that vertical transmission is rare in overtly infected modules. We show that although the parasite can occasionally infect statoblasts during overt infections, no infections were detected in the surviving mature offspring, suggesting that during overt infections, horizontal transmission incurs a trade-off with vertical transmission.

Tetracapsuloides bryosalmonae is a myxozoan parasite of freshwater bryozoans and salmonids, causing proliferative kidney disease in the latter. To date, detection of the parasite has required collection of hosts and subsequent molecular or histological examination. The release of infectious spores from both hosts offers an opportunity to detect the parasite in water samples. We developed a novel SYBR ® Green quantitative real-time PCR (qPCR) assay for T. bryosalmonae in water samples which provides an estimation of bryozoan malacospore numbers and tested the assay in 3 rivers in southern England (UK) over a period of 5 wk. The assay proved to be both highly sensitive and specific to the parasite, detecting low levels of spores throughout the study period. Larger-volume samples afforded greater detection likelihood, but did not increase the number of spores detected, possibly as a result of low and patchy spore distributions and lack of within-site replication of large-volume samples. Based on point-measurements, temperature was positively associated with the likelihood of detecting spores, possibly reflecting the temperature dependence of spore shedding from bryozoan hosts. The presence of T. bryosalmonae in water samples was predominantly influenced by spatial (sites within rivers, amongst rivers) and temporal (sampling dates) factors, while the latter also influenced quantification cycle (C q ) values and spore abundance. Environmental monitoring for infectious stages can complement traditional methods, providing faster and easier detection and avoiding potentially prolonged searching, collecting and destructive sampling of invertebrate and vertebrate hosts.

Colonial hosts offer unique opportunities for exploitation by endoparasites resulting from extensive clonal propagation, but these interactions are poorly understood. The freshwater bryozoan, Fredericella sultana, and the myxozoan, Tetracapsuloides bryosalmonae, present an appropriate model system for examining such interactions. F. sultana propagates mainly asexually, through colony fragmentation and dormant propagules (statoblasts). Our study examines how T. bryosalmonae exploits the multiple transmission routes offered by the propagation of F. sultana, evaluates the effects of such transmission on its bryozoan host, and tests the hypothesis that poor host condition provokes T. bryosalmonae to bail out of a resource that may soon be unsustainable, demonstrating terminal investment. We show that infections are present in substantial proportions of colony fragments and statoblasts over space and time and that moderate infection levels promote statoblast hatching and hence effective fecundity. We also found evidence for terminal investment, with host starvation inducing the development of transmission stages. Our results contribute to a growing picture that interactions of T. bryosalmonae and F. sultana are generally characterized by parasite persistence, facilitated by multiple transmission pathways and host condition-dependent developmental cycling, and host tolerance, promoted by effective fecundity effects and an inherent capacity for renewed growth and clonal replication.