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Vertically challenged: How disease suppresses Daphnia vertical migration behavior.

ABSTRACT: Parasitic infections are increasingly recognized as influential forces in the migratory behaviors of hosts ranging from butterflies to whales. In aquatic zooplankton, diel vertical migrations (DVMs) are among the most recurrent behaviors with implications for predator-prey interactions, nutrient cycling, and energy flow, yet how parasitism affects such migrations remains an open question. Here, we tested the effects of sporangia cluster disease (SCD) on DVM of the large-bodied Daphnia pulicaria, which is often considered a key component of lake food webs. 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 during the day, uninfected Daphnia and especially gravid individuals migrated to shallower waters at night. In contrast, infected hosts-which could comprise 40% of the population-were more likely to remain deep regardless of time of day. Among infected hosts, the intensity of SCD (sporangia count per host) predicted the degree of DVM inhibition. These observations-coupled with lab-based assays showing that infected hosts exhibited fewer swimming movements and persisted at lower depths than uninfected conspecifics-suggest that parasite-induced inhibition of DVM is a "sickness behavior" resulting from increasing morbidity and energy depletion as the infection intensifies toward host death. Considering the importance of large-bodied Daphnia as regulators of water clarity and prey for fishes, parasite-induced alterations of host migratory behavior have broad potential to affect the redistribution of energy and nutrients within lake ecosystems.

SUBMITTER: Johnson PTJ

PROVIDER: S-EPMC7377221 | biostudies-literature | 2017 Sep

REPOSITORIES: biostudies-literature

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Vertically challenged: How disease suppresses <i>Daphnia</i> vertical migration behavior.

Johnson Pieter T J PTJ Stanton Daniel E DE Forshay Kenneth J KJ Calhoun Dana M DM

Limnology and oceanography 20170901 2

Parasitic infections are increasingly recognized as influential forces in the migratory behaviors of hosts ranging from butterflies to whales. In aquatic zooplankton, diel vertical migrations (DVMs) are among the most recurrent behaviors with implications for predator-prey interactions, nutrient cycling, and energy flow, yet how parasitism affects such migrations remains an open question. Here, we tested the effects of sporangia cluster disease (SCD) on DVM of the large-bodied <i>Daphnia pulicar ...[more]

PMID: 32704187

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Project description:The antipredator behavior diel vertical migration (DVM), common in aquatic keystone species Daphnia, involves daily migration from warmer surface waters before dawn to cooler deeper waters after dusk. Plasticity in Daphnia DVM behavior optimizes fitness via trade-offs between growth, reproduction, and predator avoidance. Migration behavior is affected by co-varying biotic and abiotic factors, including light, predator cues, and anthropogenic stressors making it difficult to determine each factor's individual contribution to the variation in this behavior. This study aims to better understand this ecologically significant behavior in Daphnia by: (1) determining how Daphnia pulicaria thermal preferences vary within and among natural populations; (2) distinguishing the role of temperature verses depth in Daphnia vertical migration; and (3) defining how two anthropogenic stressors (copper and nickel) impact Daphnia migratory behavior. Simulated natural lake stratification were constructed in 8L (0.5m tall, 14.5cm wide) water columns to monitor under controlled laboratory conditions the individual effects of temperature gradients, depth, and metal stressors on Daphnia vertical migration. Three major findings are reported. First, while no difference in thermal preference was found among the four populations studied, within lake populations variability among isolates was high. Second, decoupling temperature and depth revealed that depth was a better predictor of Daphnia migratory patterns over temperature. Third, exposure to environmentally relevant concentrations of copper or nickel inhibited classic DVM behavior. These findings revealed the high variability in thermal preference found within Daphnia populations, elucidated the individual roles that depth and temperature have on migratory behavior, and showed how copper and nickel can interfere with the natural response of Daphnia to fish predator cues. Thus contributing to the body of knowledge necessary to predict how natural populations of Daphnia will be affected by climate related changes in lake temperatures and increased presence of anthropogenic stressors.

Project description:In freshwater zooplankton diel vertical migration (DVM) is a widespread predator-avoidance behavior that is induced by kairomones released from fish. Thereby zooplankton reduces predation by fish by staying in deep and dark colder strata during daytime and migrating into warmer layers during night, and thus experiences diel alterations in temperature. Constantly lower temperatures have been shown to increase the relative abundance of polyunsaturated fatty acids (PUFAs) in Daphnia sp. Furthermore, a low dietary supply of the ω3-PUFA eicosapentaenoic acid (EPA) has been shown to limit the induction of DVM in Daphnia magna and the performance of D. magna under fluctuating temperatures, as experienced during DVM. In nature DVM of D. magna in response to fish is accompanied by the presence of fish-borne kairomone and diel fluctuations of depth dependent-parameters like temperature, food, and oxygen supply. Here we investigated the effect of factors, which are differing between Daphnia that perform DVM and those which do not. We selected to examine the effect of changing temperature and light conditions and of the presence/absence of fish kairomones on D. magna. For this purpose, we conducted a full factorial experimental design in which we grew D. magna under constantly warm temperatures in a diel light-dark regime or under alternating temperatures in darkness crossed with the presence or absence of fish kairomones. We analyzed the fatty acid composition of mature animals and of their offspring in each treatment. Simulation of the light and temperature regime of migrating animals in presence of the fish kairomone resulted in an increased relative allocation of the ω3-PUFA EPA, from adult animals to their offspring, manifesting as decreased EPA concentrations in mothers and increased EPA concentrations in their offspring in response to simulated DVM (mothers). Additionally, EPA concentrations in the offspring were affected by the interaction of simulated DVM and the fish cue. The presence of the fish kairomone alone increased the EPA concentration in the offspring, that was not experiencing simulated DVM. These findings lead to the conclusion that the temperature and light regime associated with DVM alone, as well as in combination with the DVM-inducing fish kairomones, alter the allocation of fatty acids to the offspring in a manner, which is beneficial for the offspring under the decreased average temperatures, which migrating animals are exposed to. A low dietary supply of ω3-PUFAs may constrain D. magna's amplitude of DVM, but our results suggest that the next generation of animals may be capable of regaining the full DVM amplitude due to the effect of the fish kairomone and the experienced temperature fluctuations (and darkness) on tissue fatty acid composition. These findings suggest that fatty acid limitation in DVM performing Daphnia may be more severe for the maternal than for the offspring generation.

Dataset Information

Vertically challenged: How disease suppresses Daphnia vertical migration behavior.

Publications

Vertically challenged: How disease suppresses <i>Daphnia</i> vertical migration behavior.

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