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Abstract Predators can strongly influence disease transmission and evolution, particularly when they prey selectively on infected hosts. Although selective predation has been observed in numerous systems, why predators select infected prey remains poorly understood. Here, we use a mathematical model of predator vision to test a long‐standing hypothesis about the mechanistic basis of selective predation in aDaphnia–microparasite system, which serves as a model for the ecology and evolution of infectious diseases. Bluegill sunfish feed selectively onDaphniainfected by a variety of parasites, particularly in water uncolored by dissolved organic carbon. The leading hypothesis for selective predation in this system is that infection‐induced changes in the transparency ofDaphniarender them more visible to bluegill. Rigorously evaluating this hypothesis requires that we quantify the effect of infection on the visibility of prey from the predator's perspective, rather than our own. Using a model of the bluegill visual system, we show that three common parasites,Metschnikowia bicuspidata,Pasteuria ramosa, andSpirobacillus cienkowskii, decrease the transparency ofDaphnia, rendering infectedDaphniadarker against a background of bright downwelling light. As a result of this increased brightness contrast, bluegill can see infectedDaphniaat greater distances than uninfectedDaphnia—between 19% and 33% further, depending on the parasite.PasteuriaandSpirobacillusalso increase the chromatic contrast ofDaphnia. These findings lend support to the hypothesis that selective predation by fish on infectedDaphniacould result from the effects of infection onDaphnia's visibility. However, contrary to expectations, the visibility ofDaphniawas not strongly impacted by water color in our model. Our work demonstrates that models of animal visual systems can be useful in understanding ecological interactions that impact disease transmission.
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Healthy herds or predator spreaders? Insights from the plankton into how predators suppress and spread disease
How and why do predators sometimes fuel disease outbreaks but other times thwart them? Answering this could help explain spatial and temporal variation in disease and could explain why attempts to control disease by manipulating predators sometimes fail. We give eight mechanisms by which predators can suppress/spread disease in prey populations, exploring each generally and reviewing evidence from the study system that has been the focus of much of our research. This system focuses on Daphnia dentifera, a dominant herbivore in lake food webs in the Midwestern United States. D. dentifera is prey to bluegill sunfish and phantom midge larvae, as well as host to a virulent fungal pathogen. We review evidence for bluegill sunfish as ‘healthy herds’ predators that reduce disease, and for midge larvae as ‘predator spreaders’ that fuel disease outbreaks. We find that both predators can impact disease via multiple mechanisms. Bluegill feed selectively on infected hosts and also depress disease in Daphnia by reducing the density of midge larvae which spread disease. They also increase the abundance of Ceriodaphnia, which reduce disease. Midge larvae increase disease in their hosts, in part by releasing spores into the water column where they can be consumed by additional hosts.
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- Award ID(s):
- 1655856
- PAR ID:
- 10180125
- Date Published:
- Journal Name:
- Wildlife Disease Ecology: Linking theory to data and application
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract The healthy herds hypothesis proposes that predators can reduce parasite prevalence and thereby increase the density of their prey. However, evidence for such predator‐driven reductions in the prevalence of prey remains mixed. Furthermore, even less evidence supports increases in prey density during epidemics. Here, we used a planktonic predator–prey–parasite system to experimentally test the healthy herds hypothesis. We manipulated density of a predator (the phantom midge,Chaoborus punctipennis) and parasitism (the virulent fungusMetschnikowia bicuspidata) in experimental assemblages. Because we know natural populations of the prey (Daphnia dentifera) vary in susceptibility to both predator and parasite, we stocked experimental populations with nine genotypes spanning a broad range of susceptibility to both enemies. Predation significantly reduced infection prevalence, eliminating infection at the highest predation level. However, lower parasitism did not increase densities of prey; instead, prey density decreased substantially at the highest predation levels (a major density cost of healthy herds predation). This density result was predicted by a model parameterized for this system. The model specifies three conditions for predation to increase prey density during epidemics: (i) predators selectively feed on infected prey, (ii) consumed infected prey release fewer infectious propagules than unconsumed prey, and (iii) sufficiently low infection prevalence. While the system satisfied the first two conditions, prevalence remained too high to see an increase in prey density with predation. Low prey densities caused by high predation drove increases in algal resources of the prey, fueling greater reproduction, indicating that consumer–resource interactions can complicate predator–prey–parasite dynamics. Overall, in our experiment, predation reduced the prevalence of a virulent parasite but, at the highest levels, also reduced prey density. Hence, while healthy herds predation is possible under some conditions, our empirical results make it clear that the manipulation of predators to reduce parasite prevalence may harm prey density.more » « less
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ABSTRACT Predation can alter diverse ecological processes, including host–parasite interactions. Selective predation, whereby predators preferentially feed on certain prey types, can affect prey density and selective pressures. Studies on selective predation in infected populations have primarily focused on predators preferentially feeding on infected prey. However, there is substantial evidence that some predators preferentially consume uninfected individuals. Such different strategies of prey selectivity likely modulate host–parasite interactions, changing the fitness payoffs both for hosts and their parasites. Here we investigated the effects of different types of selective predation on infection dynamics and host evolution. We used a host–parasite system in the laboratory (Daphnia dentifera infected with the horizontally transmitted fungus,Metschnikowia bicuspidata) to artificially manipulate selective predation by removing infected, uninfected, or randomly selected prey over approximately 8–9 overlapping generations. We collected weekly data on population demographics and host infection and measured susceptibility from a subset of the remaining hosts in each population at the end of the experiment. After 6 weeks of selective predation pressure, we found no differences in host abundance or infection prevalence across predation treatments. Counterintuitively, populations with selective predation on infected individuals had a higher abundance of infected individuals than populations where either uninfected or randomly selected individuals were removed. Additionally, populations with selective predation for uninfected individuals had a higher proportion of individuals infected after a standardized exposure to the parasite than individuals from the two other predation treatments. These results suggest that selective predation can alter the abundance of infected hosts and host evolution.more » « less
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null (Ed.)Genetic variation in parasites has important consequences for host-parasite interactions. Prior studies of the ecologically important parasite Metschnikowia bicuspidata have suggested low genetic variation in the species. Here, we collected M. bicuspidata from two host species (Daphnia dentifera and Ceriodaphnia dubia) and two regions (Michigan and Indiana, USA). Within a lake, outbreaks tended to occur in one host species but not the other. Using microsatellite markers, we identified six parasite genotypes grouped within three distinct clades, one of which was rare. Of the two main clades, one was generally associated with D. dentifera, with lakes in both regions containing a single genotype. The other M. bicuspidata clade was mainly associated with C. dubia, with a different genotype dominating in each region. Despite these associations, both D. dentifera- and C. dubia-associated genotypes were found infecting both hosts in lakes. However, in lab experiments, the D. dentifera-associated genotype infected both D. dentifera and C. dubia, but the C. dubia-associated genotype, which had spores that were approximately 30% smaller, did not infect D. dentifera. We hypothesize that variation in spore size might help explain patterns of cross-species transmission. Future studies exploring the causes and consequences of variation in spore size may help explain patterns of infection and the maintenance of genotypic diversity in this ecologically important system.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Conference Paper:
- https://doi.org/10.1017/9781316479964.016
