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. 2015 Mar 10;112(10):3008-13.
doi: 10.1073/pnas.1415971112. Epub 2015 Feb 23.

Predator diversity, intraguild predation, and indirect effects drive parasite transmission

Affiliations

Predator diversity, intraguild predation, and indirect effects drive parasite transmission

Jason R Rohr et al. Proc Natl Acad Sci U S A. .

Abstract

Humans are altering biodiversity globally and infectious diseases are on the rise; thus, there is interest in understanding how changes to biodiversity affect disease. Here, we explore how predator diversity shapes parasite transmission. In a mesocosm experiment that manipulated predator (larval dragonflies and damselflies) density and diversity, non-intraguild (non-IG) predators that only consume free-living cercariae (parasitic trematodes) reduced metacercarial infections in tadpoles, whereas intraguild (IG) predators that consume both parasites and tadpole hosts did not. This likely occurred because IG predators reduced tadpole densities and anticercarial behaviors, increasing per capita exposure rates of the surviving tadpoles (i.e., via density- and trait-mediated effects) despite the consumption of parasites. A mathematical model demonstrated that non-IG predators reduce macroparasite infections, but IG predation weakens this "dilution effect" and can even amplify parasite burdens. Consistent with the experiment and model, a wetland survey revealed that the diversity of IG predators was unrelated to metacercarial burdens in amphibians, but the diversity of non-IG predators was negatively correlated with infections. These results are strikingly similar to generalities that have emerged from the predator diversity-pest biocontrol literature, suggesting that there may be general mechanisms for pest control and that biocontrol research might inform disease management and vice versa. In summary, we identified a general trait of predators--where they fall on an IG predation continuum--that predicts their ability to reduce infections and possibly pests in general. Consequently, managing assemblages of predators represents an underused tool for the management of human and wildlife diseases and pest populations.

Keywords: biodiversity–ecosystem function; dilution effect; schistosomiasis; snail; trophic cascade.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
The relationship between the taxonomic richness of potential cercarial predators in a wetland and the number of metacercariae per frog per wetland (A), effects of the density of I. verticalis on the survival of R. clamitans tadpoles in a mesocosm experiment (B), and the standardized slope parameters (±1 SE) between the number of metacercariae per frog per wetland and either the taxonomic richness of non-IG (those that only eat cercariae) or IG predators (those that regularly eat cercariae and tadpoles) in a wetland (C) (see A for the relationship of the two groups combined). In the scatterplots, best-fit lines and 95% confidence bands are presented.
Fig. 2.
Fig. 2.
Results of the mesocosm experiment showing effects of larval odonate density (0, 6, or 12 individuals; ○しろまる, □しろいしかく, and ■しかく, respectively) and diversity (zero to three species) on (A) metacercarial infections per tadpole, (B) tadpole survival (i.e., density), and (C) tadpole activity. Shown are means ±1 SE. See text for sample sizes and statistics.
Fig. 3.
Fig. 3.
Relationships between metacercariae per tadpole and the densities of two non-IG predators (those that only eat cercariae), (A) S. semicinctum and (B) P. longipennis and (C) an IG-predator (eats cercariae and tadpoles), I. verticalis. Shown are the predicted values from a model with temporal block and the main effects of each species, the presence-only treatments for each species, and best-fit lines for significant relationships.
Fig. 4.
Fig. 4.
Relationships between tadpole activity and metacercarial infections in R. clamitans tadpoles. (A) Effects of two non-IG predators (those that only eat cercariae), S. semicinctum and P. longipennis, and an IG-predator (eats cercariae and tadpoles), I. verticalis, in monospecific treatments on tadpole activity. Points with different letters are significantly different from one another (P < 0.05). (B) Tadpole activity and metacercarial loads as a function of the density of the IG predator I. verticalis, the only odonate species that significantly reduced tadpole activity. (C) Relationship between tadpole activity in treatments with I. verticalis and metacercarial infections per tadpole. The first number next to each point represents the number of I. verticalis in that treatment and the second number represents the total number of odonate larvae in that treatment. In each panel, means and 1 SE are displayed.
Fig. 5.
Fig. 5.
Epidemiological consequences of simultaneous predation on focal hosts and free-living parasites (correspond with tadpoles and cercariae in our experimental system) at equilibrial values. (A) Increasing predation on free-living parasites increases the equilibrium density of focal hosts. However, increasing predation on focal hosts strongly reduces their equilibrium density. (B) Both types of predation reduce the equilibrial density of parasitic infections within focal hosts. (C) Predation on free-living parasites causes a monotonic decrease in equilibrial mean burden of infection for individual focal hosts. In contrast, predation on focal hosts causes a unimodal response. Initially, predation on focal hosts slightly reduces mean burdens. However, as predation on focal hosts increases, equilibrial mean burden rises, eventually surpassing burdens in the absence of predation. Thus, predators of free-living parasites monotonically reduce mean burdens for definitive hosts. However, predators of focal hosts can only weakly reduce mean burden or even amplify infection risk for hosts. Simulation parameters are identical to those in Fig. S4.

References

    1. Jones KE, et al. Global trends in emerging infectious diseases. Nature. 2008;451(7181):990–993. - PMC - PubMed
    1. Olden JD, Leroy Poff N, Douglas MR, Douglas ME, Fausch KD. Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol. 2004;19(1):18–24. - PubMed
    1. Dobson A, et al. Sacred cows and sympathetic squirrels: The importance of biological diversity to human health. PLoS Med. 2006;3(6):e231. - PMC - PubMed
    1. Keesing F, et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature. 2010;468(7324):647–652. - PMC - PubMed
    1. Keesing F, Holt RD, Ostfeld RS. Effects of species diversity on disease risk. Ecol Lett. 2006;9(4):485–498. - PubMed

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