Parasites destabilize host populations by shifting stage-structured interactions: An evaluation combining models, experiments, and field data

Background/Question/Methods

Should parasites stabilize or destabilize consumer-resource dynamics? Recent theoretical findings suggest that disease-induced mortality should be a stabilizing force. This possibility is intriguing because disease is ubiquitous in consumer populations — perhaps parasites confer greatly underappreciated stability to their hosts in natural ecosystems. In some consumer/host-resource-disease models, disease induced mortality of the host-consumer prevents severe over-exploitation of the host’s resource. As a result, the resource’s own negative density dependence enhances stability of the system. We looked for the signature of these predictions using a case study of consumer-host Daphnia and a fungal parasite. Hypothesis 1: Disease imposed mortality stabilizes: We expected that (1) per capita death rate should increase with epidemic size, thus, (2) host populations should fluctuate less during larger epidemics. Death rate increased with epidemic size; however, larger epidemics correlated with larger — not smaller — fluctuations of the consumer-host. Seeking resolution to this model-nature discrepancy, we looked for key biology missing from existing models that might explain why disease should destabilize — or appear to destabilize — a consumer/host-resource system. We investigated two additional hypotheses. Hypothesis 2 Ecosystem productivity destabilizes: nutrients could merely create a positive correlation between epidemic size and instability through paradox of enrichment type mechanisms. Hypothesis 3 Host stage-structure: disease-mediated changes in competitive interactions between juvenile and adult hosts shift host populations from relatively stable, asynchronous cycles to less stable (i.e., higher variation), synchronized cycles.

Results/Conclusions

Across 16 lakes, host populations became less stable as epidemic size increased and host stage dynamics became synchronized. Epidemic size and changes in stability, however, were both correlated with ecosystem productivity (indexed by total phosphorous). Two population-level experiments then confirmed that disease, not nutrients, destabilized host populations and synchronized dynamics between juvenile and adult stages (characterized by variability indices and time series analyses). What underlying mechanisms link stage-structure and disease? Stage-structure theory and previous results in this system suggest asymmetric effects of resources and disease on host stages. These asymmetric effects arise, in part, because host foraging rates - and thus exposure - increase with body size and vary depending on resource quantity and quality. Thus, disease that predominantly affects adults — as in numerous disease systems — can place juveniles and adults on more equal competitive footing and alter host population stability. Our study highlights that connecting stage-structured interactions with epidemiologically relevant processes (e.g., consumption-based exposure) may greatly enhance our understanding of when and how parasites alter host population stability.