Co-infecting parasites: How parasite assemblages and timing of exposure affect host pathology and parasite loads

Background/Question/Methods

Within natural communities, hosts are exposed to an assemblage of parasite species that form a complex community within the host.  Such co-infecting parasites can interact in a variety of direct (e.g., competition for attachment sites) and indirect (e.g., host-mediated cross immunity) ways that ultimately affect host pathology, parasite load, and parasite transmission.  Over 400 species of digenetic trematodes (flukes) infect amphibians as part of their life cycle.  Recently, some of these parasites have gained notoriety for their capacity to induce severe pathology and limb deformities in amphibians.  In order to understand parasite community ecology in this system, we conducted broad-scale field surveys to characterize natural patterns in parasite community structure and controlled experiments to identify the mechanisms underlying this structure.  

Results/Conclusions

In our surveys of 97 ponds in the Bay area of California, parasites exhibited strongly nested patterns within Pacific chorus frog hosts, with low-diversity communities representing near-perfect subsets of more diverse communities.  To assess the potential mechanisms underlying this structure and the consequences for amphibian pathology and parasite loads, we conducted controlled laboratory experiments that manipulated parasite assemblages and the timing of parasite exposure.  Focusing on two of the most pathogenic parasites (Ribeiroia ondatrae and Echinostoma trivolvis), we found that increases in parasite species richness had significant negative effects on recovery of each parasite.  Given that these parasites form cysts in different regions of the body, these results suggest that increases in parasite species richness exerted indirect negative effects upon the infection success of one another, likely via cross immunity (apparent competition).   However, when we altered the timing of parasite exposure, we found that previously established parasites had little influence on the recovery of later colonizing parasites.  This suggests that the timing of exposure can ameliorate apparent competition.  Moreover, there were significant effects of exposure timing on recovery for each parasite species.  In particular, recovery was greater in tadpoles exposed earlier in development due to reduced resistance to infection.  As a consequence of these changes in host resistance over development, exposure timing significantly affected the total parasite load in the hosts.  Together, these results suggest that parasite assemblages are influenced by multiple factors including the timing of exposure, species richness in the system, and developmental changes in host resistance.  Our study underscores the need for integrating field survey and experimental studies to understand the mechanisms generating parasite assembly.