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Vertically challenged: How disease suppresses Daphnia vertical migration behavior
Citation:
Johnson, P., D. Stanton, Ken Forshay, AND D. Calhoun. Vertically challenged: How disease suppresses Daphnia vertical migration behavior. LIMNOLOGY AND OCEANOGRAPHY. American Society of Limnology and Oceanography, Lawrence, KS, , 1-11, (2017). https://doi.org/10.1002/lno.10676
Impact/Purpose:
An exciting nexus in ecology is the recent synergism between research on animal migrations and the disease-induced effects on host behaviors. Because parasites and pathogens often have sublethal effects on host behavior, fecundity, and mobility, the ‘hidden’ role of infection for understanding both small- and large-scale animal movement patterns has attracted growing attention. One of the persistent challenges in understanding observed links between infection and migration is the difficulty in testing their underlying processes, particularly when large spatial scales involved. For instance, do migratory hosts exhibit more (or less) infection owing to differences in environmental exposure, variation in transmission conditions (e.g., host aggregation), or differences in host survival during or prior to migratory movements? Here we capitalize on the highly predictable daily movement patterns of zooplankton (i.e., diel vertical migrations, DVM), which have been extensively studied in limnology and occur at a tractable scale to allow rigorous testing of alternative hypotheses. Building from disease theory and previous literature, we expected that infected hosts might exhibit diminished or even reversed DVM behavior, consistent with ‘sickness behaviors’ or ‘parasite manipulation’, respectively. Over two years, we characterized how patterns of infection by the highly pathogenic chyrid fungus Polycaryum laevae in large-bodied Daphnia pulicara varied by depth, time of day, and over the season to determine whether infection caused differential DVM behaviors. We also tested how host-level characteristics, including infection intensity, fecundity, and body size, interacted to determine the vertical position of >30,000 hosts. We coupled these samples with an examination of archived collections from a second lake known to have low planktivory (and thus less pronounced DVM), helping to comparatively assess the potential role of ‘missing samples’ due to predation. Finally, we performed laboratory-assays with infected and uninfected Daphnia to test for differences in vertical position and swimming behavior in the absence of environmental variation. Our results demonstrate that infected and uninfected Daphnia exhibit stark differences in vertical migration. While all hosts tended to remain low in the water column during the day, uninfected Daphnia and especially gravid females migrated to shallower waters at night. Infected hosts, however, spent more of their time deep in the lake, even during nocturnal periods when predation threats from fishes were minimized, and this effect became more pronounced with infection severity (spores per host). Correspondingly, at the lake with low planktivory, this difference in vertical distribution was evident even during daylight samples collected over a three-month period. These observations – coupled with lab-based measurements showing that infected hosts exhibited fewer swimming movements and persisted at lower depths than uninfected conspecifics – suggest that the observed alterations in DVM are a ‘sickness behavior,’ most likely resulting from increasing morbidity and energy depletion as the infection progresses toward host death. Considering the importance of large-bodied Daphnia as regulators of water clarity and prey for fishes, parasite-induced alterations of host behavior have broad potential to affect ecological processes in lakes.
Description:
Parasite infections and the resulting forms of disease pathology are increasingly recognized as influential forces in the migratory behaviors of hosts ranging from butterflies to whales. In aquatic zooplankton, diel vertical migrations (DVM) are among the most recurrent behaviors with implications for predator-prey interactions, nutrient cycling, and energy flow, yet how parasitism affects this pattern remains an open question. Here we tested the effects of Sporangia Cluster Disease (SCD) on the DVM behavior of the large-bodied daphnid Daphnia pulicaria, which is an important component of many lake food webs. Caused by the chytridiomycete Polycaryum laeve, SCD leads to reduced growth, reproductive castration, and eventually death of the host. By collecting depth-specific zooplankton samples across diel cycles, between years, and among lakes, we show that infection is associated with strong inhibition of host DVM; while all Daphnia tended to occur deeper in the lake during the day, infected hosts were more likely to remain deep at night, whereas uninfected Daphnia and especially gravid individuals migrated to shallower water. Among infected hosts, the intensity of SCD (sporangia count per host) further predicted the degree of DVM inhibition. Laboratory-based assays of host swimming activity indicated that infected individuals exhibited 17% fewer swimming movements and occurred at lower (deeper) vertical positions in observation chambers relative to uninfected conspecifics. Considering the importance of large-bodied Daphnia as regulators of water clarity and prey for fishes, parasite-induced alterations of host behavior have broad potential to affect ecological processes in lakes.
URLs/Downloads:
DOI: Vertically challenged: How disease suppresses Daphnia vertical migration behavior
Free access through PubMed Central
https://www.researchgate.net/publication/319592577