An official website of the United States government
Environmental temperature fundamentally shapes insect physiology, fitness and interactions with parasites. Differential climate warming effects on host versus parasite biology could exacerbate or inhibit parasite transmission, with far-reaching implications for pollination services, biocontrol and human health. Here, we experimentally test how controlled temperatures influence multiple components of host and parasite fitness in monarch butterflies (Danaus plexippus) and their protozoan parasitesOphryocystis elektroscirrha. Using five constant-temperature treatments spanning 18–34°C, we measured monarch development, survival, size, immune function and parasite infection status and intensity. Monarch size and survival declined sharply at the hottest temperature (34°C), as did infection probability, suggesting that extreme heat decreases both host and parasite performance. The lack of infection at 34°C was not due to greater host immunity or faster host development but could instead reflect the thermal limits of parasite invasion and within-host replication. In the context of ongoing climate change, temperature increases above current thermal maxima could reduce the fitness of both monarchs and their parasites, with lower infection rates potentially balancing negative impacts of extreme heat on future monarch abundance and distribution.
more »
« less
Temperature and Resources Interact to Affect Transmission via Host Foraging Rate and Susceptibility
ABSTRACT Environmental conditions such as temperature and resource availability can shape disease transmission by altering contact rates and/or the probability of infection given contact. However, interactive effects of these factors on transmission processes remain poorly understood. We develop mechanistic models and fit them to experimental data to uncover how temperature and resources jointly affect transmission of fungal parasites (Metschnikowia bicuspidata) in zooplankton hosts (Daphnia dentifera). Model competition revealed interactive effects of temperature and resources on both contact rates (host foraging) and the probability of infection given contact (per‐parasite susceptibility). Foraging rates increased with temperature and decreased with resources (via type‐II functional response), but this resource effect weakened at warmer temperatures due to shorter handling times. Per‐parasite susceptibility increased with resources at cooler temperatures but remained consistently high when warmer. Our analysis demonstrates that temperature and resources interact to shape transmission processes and provides a general theoretical framework for other host–parasite systems.
more »
« less
- Award ID(s):
- 2245422
- PAR ID:
- 10609002
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Ecology Letters
- Volume:
- 28
- Issue:
- 6
- ISSN:
- 1461-023X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Pesticide pollution can alter parasite transmission, but scientists are unaware if effects of pesticides on parasite exposure and host susceptibility (i.e. infection risk given exposure) can be generalised within a community context. Using replicated temperate pond communities, we evaluate effects of 12 pesticides, nested in four pesticide classes (chloroacetanilides, triazines, carbamates organophosphates) and two pesticide types (herbicides, insecticides) applied at standardised environmental concentrations on larval amphibian exposure and susceptibility to trematode parasites. Most of the variation in exposure and susceptibility occurred at the level of pesticide class and type, not individual compounds. The organophosphate class of insecticides increased snail abundance (first intermediate host) and thus trematode exposure by increasing mortality of snail predators (top–down mechanism). While a similar pattern in snail abundance and trematode exposure was observed with triazine herbicides, this effect was driven by increases in snail resources (periphytic algae, bottom–up mechanism). Additionally, herbicides indirectly increased host susceptibility and trematode infections by (1) increasing time spent in susceptible early developmental stages and (2) suppressing tadpole immunity. Understanding generalisable effects associated with contaminant class and type on transmission is critical in reducing complexities in predicting disease dynamics in at‐risk host populations.more » « less
-
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
-
Can hot temperatures limit disease transmission? A test of mechanisms in a zooplankton–fungus systemAbstract 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.more » « less
-
Abstract Predation on parasites is a common interaction with multiple, concurrent outcomes. Free‐living stages of parasites can comprise a large portion of some predators' diets and may be important resources for population growth. Predation can also reduce the density of infectious agents in an ecosystem, with resultant decreases in infection rates. While predator–parasite interactions likely vary with parasite transmission strategy, few studies have examined how variation in transmission mode influences contact rates with predators and the associated changes in consumption risk.To understand how transmission mode mediates predator–parasite interactions, we examined associations between an oligochaete predatorChaetogaster limnaeithat lives commensally on freshwater snails and nine trematode taxa that infect snails.Chaetogasteris hypothesized to consume active (i.e. mobile), free‐living stages of trematodes that infect snails (miracidia), but not the passive infectious stages (eggs); it could thus differentially affect transmission and infection prevalence of parasites, including those with medical or veterinary importance. Alternatively, when infection does occur,Chaetogastercan consume and respond numerically to free‐living trematode stages released from infected snails (cercariae). These two processes lead to contrasting predictions about whetherChaetogasterand trematode infection of snails correlate negatively (‘protective predation’) or positively (‘predator augmentation’).Here, we tested how parasite transmission mode affectedChaetogaster–trematode relationships using data from 20,759 snails collected across 4 years from natural ponds in California. Based on generalized linear mixed modelling, snails with moreChaetogasterwere less likely to be infected by trematodes that rely on active transmission. Conversely, infections by trematodes with passive infectious stages were positively associated with per‐snailChaetogasterabundance.Our results suggest that trematode transmission mode mediates the net outcome of predation on parasites. For trematodes with active infectious stages, predatoryChaetogasterlimited the risk of snail infection and its subsequent pathology (i.e. castration). For taxa with passive infectious stages, no such protective effect was observed. Rather, infected snails were associated with higherChaetogasterabundance, likely owing to the resource subsidy provided by cercariae. These findings highlight the ecological and epidemiological importance of predation on free‐living stages while underscoring the influence of parasite life history in shaping such interactions.more » « less
