Do defensive symbionts indirectly alter parasite transmission to hosts without defensive symbionts?

Background/Question/Methods

Many important parasites of humans, livestock, and wildlife have complex life cycles that include a free-living stage in which the parasites exist in the environment outside of the host.  Predators of these free-living parasite stages have recently gained increasing attention for their potential to reduce parasite transmission.  Here, we considered a symbiotic annelid (Chaetogaster limnaei limnaei) of freshwater snails that is a predator of free-living larval trematode parasites.  Laboratory experiments have repeatedly demonstrated that Chaetogaster substantially reduce trematode infection in their snail hosts.  Observations during laboratory experiments also suggested that in addition to directly reducing snail infection by consuming larval trematodes, Chaetogaster may indirectly influence trematode transmission dynamics by deterring trematodes from infecting Chaetogaster-infested snails.  This might cause potential trematode hosts without Chaetogaster, such as tadpoles, to experience increased trematode infection.  To test this hypothesis, we performed a mesocosm experiment in which larval trematodes were added to mesocosms that contained tadpoles alone, tadpoles and snails, or tadpoles and Chaetogaster-infested snails.  If Chaetogaster indirectly influenced trematode transmission, we expected that tadpoles in mesocosms with Chaetogaster-infested snails would have higher per capita infection rates by trematodes than tadpoles in the other treatment groups.      

Results/Conclusions

In accordance with existing laboratory experiments, Chaetogaster directly reduced the intensity of snail infection by 64% in mesocosms. However, contrary to our prediction, Chaetogaster did not indirectly affect trematode transmission: tadpole infection was not significantly different across treatment groups with and without Chaetogaster.  We suggest that future work considering the downstream consequences of the direct reduction in snail infection will be more important to understanding trematode transmission dynamics than further work considering the lateral, indirect effects of Chaetogaster.  Finally, we found that snails infested with Chaetogaster had reduced growth rates in comparison to snails without Chaetogaster.  This may indicate that Chaetogaster can act as a mutualist of snails – by reducing trematode infection – and also potentially as a parasite of snails, by reducing snail growth.  The long-term net effects of Chaetogaster on snail population dynamics remains a fascinating topic for future study.