The effects of phylogeny, habitat and host characteristics on the thermal sensitivity of helminth development

Abstract

Helminth parasites are part of almost every ecosystem, with more than 300 000 species worldwide. Helminth infection dynamics are expected to be altered by climate change, but predicting future changes is difficult owing to lacking thermal sensitivity data for greater than 99.9% of helminth species. Here, we compiled the largest dataset to date on helminth temperature sensitivities and used the Metabolic Theory of Ecology to estimate activation energies (AEs) for parasite developmental rates. The median AE for 129 thermal performance curves was 0.67, similar to non-parasitic animals. Although exceptions existed, related species tended to have similar thermal sensitivities, suggesting some helminth taxa are inherently more affected by rising temperatures than others. Developmental rates were more temperature-sensitive for species from colder habitats than those from warmer habitats, and more temperature sensitive for species in terrestrial than aquatic habitats. AEs did not depend on whether helminth life stages were free-living or within hosts, whether the species infected plants or animals, or whether the species had an endotherm host in its life cycle. The phylogenetic conservatism of AE may facilitate predicting how temperature change affects the development of helminth species for which empirical data are lacking or difficult to obtain.

Keywords: activation energy; climate change; metabolic theory; parasite.

Figure 1.

Distribution of activation energy (AE) estimates (n = 129) for the development rate of 87 helminth species. AE was estimated using the Sharpe-Schoolfield model (SS) when thermal performance curves had an unambiguous peak and using the Boltzmann-Arrhenius model (BA) otherwise. The arrow indicates the median. The solid line is an overall density line, calculated for all AE estimates, regardless of whether they were estimated with the BA or SS model. (Online version in colour.)

Figure 2.

Phylogenetic structure in activation energy (AE) estimates for 87 helminth species. AE is colour coded, with tips showing median species values and nodes depicting predictions from a phylogenetic mixed model. (Online version in colour.)

Figure 3.

Activation energy (AE) of helminth development as a function of four environmental variables: (a) mean annual temperature of the parasite's sampling locale, (b) range in monthly mean temperatures, (c) latitude, and (d) habitat. Point diameter is proportional to the inverse standard error of the AE estimate and thus reflects its weight in the analysis. Lines and shaded areas represent best fits and credible intervals from mixed models, including parasite phylogeny and the other environmental variables.

Figure 4.

Activation energy (AE) of helminth development separated by host types (animal parasites with and without an endotherm in their life cycle and plant parasites) and whether the studied parasite stage was inside a host or outside in the external environment. Point diameter reflects its weight in the analysis, i.e. the inverse standard error of the AE estimate. Lines and shaded areas represent estimated means and credible intervals from mixed models accounting for parasite phylogeny. (Online version in colour.)