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Abstract Understanding parasite transmission in communities requires knowledge of each species' capacity to support transmission. This property, ‘competence’, is a critical currency for modelling transmission under community change and for testing diversity–disease theory. Despite the central role of competence in disease ecology, we lack a clear understanding of the factors that generate competence and drive its variation.We developed novel conceptual and quantitative approaches to systematically quantify competence for a multi‐host, multi‐parasite community. We applied our framework to an extensive dataset: five amphibian host species exposed to four parasitic trematode species across five ecologically realistic exposure doses. Together, this experimental design captured 20 host–parasite interactions while integrating important information on variation in parasite exposure. Using experimental infection assays, we measured multiple components of the infection process and combined them to produce competence estimates for each interaction.With directly estimated competence values, we asked which components of the infection process best explained variation in competence: barrier resistance (the initial fraction of administered parasites blocked from infecting a host), internal clearance (the fraction of established parasites lost over time) or pre‐transmission mortality (the probability of host death prior to transmission). We found that variation in competence among the 20 interactions was best explained by differences in barrier resistance and pre‐transmission mortality, underscoring the importance of host resistance and parasite pathogenicity in shaping competence.We also produced dose‐integrated estimates of competence that incorporated natural variation in exposure to address questions on the basis and extent of variation in competence. We found strong signals that host species identity shaped competence variation (as opposed to parasite species identity). While variation in infection outcomes across hosts, parasites, individuals and doses was considerable, individual heterogeneity was limited compared to among‐species differences. This finding highlights the robustness of our competence estimates and suggests that species‐level values may be strong predictors for community‐level transmission in natural systems.Competence emerges from distinct underlying processes and can have strong species‐level characteristics; thus, this property has great potential for linking mechanisms of infection to epidemiological patterns. Read the freePlain Language Summaryfor this article on the Journal blog.
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Can hot temperatures limit disease transmission? A test of mechanisms in a zooplankton–fungus system
Abstract Thermal ecology theory predicts that transmission of infectious diseases should respond unimodally to temperature, that is be maximized at intermediate temperatures and constrained at extreme low and high temperatures. However, empirical evidence linking hot temperatures to decreased transmission in nature remains limited.We tested the hypothesis that hot temperatures constrain transmission in a zooplankton–fungus (Daphnia dentifera–Metschnikowia bicuspidata) disease system where autumnal epidemics typically start after lakes cool from their peak summer temperatures. This pattern suggested that maximally hot summer temperatures could be inhibiting disease spread.Using a series of laboratory experiments, we examined the effects of high temperatures on five mechanistic components of transmission. We found that (a) high temperatures increased exposure to parasites by speeding up foraging rate but (b) did not alter infection success post‐exposure. (c) High temperatures lowered parasite production (due to faster host death and an inferred delay in parasite growth). (d) Parasites made in hot conditions were less infectious to the next host (instilling a parasite ‘rearing’ or 'trans‐host' effect of temperature during the prior infection). (e) High temperatures in the free‐living stage also reduce parasite infectivity, either by killing or harming parasites.We then assembled the five mechanisms into an index of disease spread. The resulting unimodal thermal response was most strongly driven by the rearing effect. Transmission peaked at intermediate hot temperatures (25–26°C) and then decreased at maximally hot temperatures (30–32°C). However, transmission at these maximally hot temperatures only trended slightly lower than the baseline control (20°C), which easily sustains epidemics in laboratory conditions and in nature. Overall, we conclude that while exposure to hot epilimnetic temperatures does somewhat constrain disease, we lack evidence that this effect fully explains the lack of summer epidemics in this natural system. This work demonstrates the importance of experimentally testing hypothesized mechanisms of thermal constraints on disease transmission. Furthermore, it cautions against drawing conclusions based on field patterns and theory alone. A freePlain Language Summarycan be found within the Supporting Information of this article.
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- Award ID(s):
- 1655656
- PAR ID:
- 10458353
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Functional Ecology
- Volume:
- 33
- Issue:
- 10
- ISSN:
- 0269-8463
- Page Range / eLocation ID:
- p. 2017-2029
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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