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      The sicker the better: nematode-infected passalus beetles provide enhanced ecosystem services

      1 , 1
      Biology Letters
      The Royal Society

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          Abstract

          There is growing appreciation for the role that parasites have in ecosystems and food webs, though the possibility that they could improve an ecosystem service has never been considered. In forest ecosystems, fallen trees naturally decay over time and slowly return their nutrients to the soil. Beetles in the family Passalidae play a key role by excavating tunnels and consuming wood from these logs, thereby breaking down the wood into smaller debris. In the eastern United States, the horned passalus (Odontotaenius disjunctus) is host to a naturally occurring nematode, Chondronema passali, which appears to cause little harm to the beetles. We suspected this was due to compensatory food consumption by parasitized individuals, which we tested here. We collected and housed 113 adult beetles in individual containers with wood for three months, then determined the amount of wood each beetle had processed into fine debris and frass. We then assessed beetles for C. passali and compared wood processing rates between parasitized and non-parasitized groups. Results showed the average daily processing rate of parasitized beetles ( x ¯ = 0.77 g d−1) was 15% greater than that of unparasitized ones ( x ¯ = 0.67 g d−1). Parasitized beetles were 6% larger, and this may explain some of this pattern, though the effect of parasitism was still significant in our analysis. By extrapolating the daily rates, we estimate that 10 adult beetles without nematodes would break down approximately 2.4 kg of wood in a single year, while a group of 10 parasitized beetles would break down 2.8 kg. While our data are consistent with the idea of compensatory feeding, because these results are based on natural infections, we cannot rule out the possibility that beetles with heightened wood consumption are simply more likely to acquire the parasite. At an ecosystem level, it may not matter which is the case; parasitized beetles provide a more effective ecosystem service.

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          Most cited references17

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          A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health.

          Honey bee colony losses are triggered by interacting stress factors consistently associated with high loads of parasites and/or pathogens. A wealth of biotic and abiotic stressors are involved in the induction of this complex multifactorial syndrome, with the parasitic mite Varroa destructor and the associated deformed wing virus (DWV) apparently playing key roles. The mechanistic basis underpinning this association and the evolutionary implications remain largely obscure. Here we narrow this research gap by demonstrating that DWV, vectored by the Varroa mite, adversely affects humoral and cellular immune responses by interfering with NF-κB signaling. This immunosuppressive effect of the viral pathogen enhances reproduction of the parasitic mite. Our experimental data uncover an unrecognized mutualistic symbiosis between Varroa and DWV, which perpetuates a loop of reciprocal stimulation with escalating negative effects on honey bee immunity and health. These results largely account for the remarkable importance of this mite-virus interaction in the induction of honey bee colony losses. The discovery of this mutualistic association and the elucidation of the underlying regulatory mechanisms sets the stage for a more insightful analysis of how synergistic stress factors contribute to colony collapse, and for the development of new strategies to alleviate this problem.
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            Diverse effects of parasites in ecosystems: linking interdependent processes

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              Eating yourself sick: transmission of disease as a function of foraging ecology.

              Species interactions may profoundly influence disease outbreaks. However, disease ecology has only begun to integrate interactions between hosts and their food resources (foraging ecology) despite that hosts often encounter their parasites while feeding. A zooplankton-fungal system illustrated this central connection between foraging and transmission. Using experiments that varied food density for Daphnia hosts, density of fungal spores and body size of Daphnia, we produced mechanistic yet general models for disease transmission rate based on broadly applicable components of feeding biology. Best performing models could explain why prevalence of infection declined at high food density and rose sharply as host size increased (a pattern echoed in nature). In comparison, the classic mass-action model for transmission performed quite poorly. These foraging-based models should broadly apply to systems in which hosts encounter parasites while eating, and they will catalyse future integration of the roles of Daphnia as grazer and host.
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                Author and article information

                Journal
                Biology Letters
                Biol. Lett.
                The Royal Society
                1744-9561
                1744-957X
                May 31 2019
                May 31 2019
                : 15
                : 5
                : 20180842
                Affiliations
                [1 ]Odum School of Ecology, University of Georgia, Athens, GA 30602, USA
                Article
                10.1098/rsbl.2018.0842
                6548735
                31039727
                dc2df419-772f-495c-9cf0-304a703d72a5
                © 2019
                History

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