The energetic costs of sub‐lethal helminth parasites in mammals: a meta‐analysis

Abstract

Parasites, by definition, have a negative effect on their host. However, in wild mammal health and conservation research, sub-lethal infections are commonly assumed to have negligible health effects unless parasites are present in overwhelming numbers. Here, we propose a definition for host health in mammals that includes sub-lethal effects of parasites on the host's capacity to adapt to the environment and maintain homeostasis. We synthesized the growing number of studies on helminth parasites in mammals to assess evidence for the relative magnitude of sub-lethal effects of infection across mammal taxa based on this expanded definition. Specifically, we develop and apply a framework for organizing disparate metrics of parasite effects on host health and body condition according to their impact on an animal's energetic condition, defined as the energetic burden of pathogens on host physiological and behavioural functions that relate directly to fitness. Applying this framework within a global meta-analysis of helminth parasites in wild, laboratory and domestic mammal hosts produced 142 peer-reviewed studies documenting 599 infection-condition effects. Analysing these data within a multiple working hypotheses framework allowed us to evaluate the relative weighted contribution of methodological (study design, sampling protocol, parasite quantification methods) and biological (phylogenetic relationships and host/parasite life history) moderators to variation in the magnitude of health effects. We found consistently strong negative effects of infection on host energetic condition across taxonomic groups, with unusually low heterogeneity in effect sizes when compared with other ecological meta-analyses. Observed effect size was significantly lower within crosssectional studies (i.e. observational studies that investigated a sub-set of a population at a single point in time), the most prevalent methodology. Furthermore, opportunistic sampling led to a weaker negative effect compared to proactive sampling. In the model of host taxonomic group, the effect of infection on energetic condition in carnivores was not significant. However, when sampling method was included, it explained substantial inter-study variance; proactive sampling showing a strongly significant negative effect while opportunistic sampling detected only a weak, non-significant effect. This may partly underlie previous assumptions that sub-lethal parasites do not have significant effects on host health. We recommend future studies adopt energetic condition as the framework for assessing parasite effects on wildlife health and provide guidelines for the selection of research protocols, health proxies, and relating infection to fitness.

Meta‐analysis suggests that, for marine mammals, the risk of parasitism by anisakids changed between 1978 and 2015

“…Marine mammals have high energetic demands (Berta, 2020; McNab, 2012), and populations that are declining due to persistent sublethal stressors, like acoustic or physical disturbance, entanglement, or bioaccumulation of pollutants, are likely to face elevated energy demands (Berta, 2020; King et al, 2015; McNab, 1989, 2012). This can result in individuals having less energy available to devote to immune response, making them more susceptible to infection (Beldomenico et al, 2008; Shanebeck et al, 2022; e.g., Colegrove et al, 2016; Lair et al, 2016; Seguel et al, 2018). It also leaves less energy to spare, meaning that the energetic costs of parasite infection could have population‐level consequences (Beldomenico et al, 2008; King et al, 2015; May et al, 2019; Shanebeck et al, 2022).…”

“…This can result in individuals having less energy available to devote to immune response, making them more susceptible to infection (Beldomenico et al, 2008; Shanebeck et al, 2022; e.g., Colegrove et al, 2016; Lair et al, 2016; Seguel et al, 2018). It also leaves less energy to spare, meaning that the energetic costs of parasite infection could have population‐level consequences (Beldomenico et al, 2008; King et al, 2015; May et al, 2019; Shanebeck et al, 2022). Meanwhile, healthy marine mammal populations with few stressors may increase in abundance and continue to tolerate parasite infections, further serving as breeding grounds for parasites and possibly increasing the population of infectious helminths available to infect more vulnerable hosts.…”

“…In severe infections, the perforations of the stomach wall can cause peritonitis, ultimately leading to hemorrhaging, anemia, and, rarely, death (Ballachey et al, 2002; Dailey, 1985; Dailey & Stroud, 1978; Margolis et al, 1997; Smith, 1989; Stroud & Roffe, 1979; van Beurden et al, 2015). Whether or not these infections result in disease or mortality, they reduce the hosts' fitness, which can have individual and population‐level consequences (Shanebeck et al, 2022).…”

Host condition, seasonality and environmental factors explain parasite community differences between urban and rural foxes

“…Body condition can be impacted by helminths or -in the opposite causal direction -helminths can infect primarily the weakest, most susceptible individuals in a population opportunistically. The support for such negative associations between body condition and helminth loads have been shown to be surprisingly robust across study systems, albeit with lower support in carnivores, in a recent meta-analysis (Shanebeck et al 2022). Reduced body weight and diverse co-infections are likely both a cause and a consequence of each other in a "vicious circle" (Beldomenico et al 2008).…”

Effects of the invasive swim bladder parasiteAnguillicola crassuson health and condition indicators in the European eel

“…We predicted that infected eels would have a larger relative spleen size, as a sign of an active immune response to parasitism (Lamková et al, 2007;Ottová et al, 2007;Owens & Wilson, 1999), and a smaller relative liver size due to parasite-related depletion of the energy reserve typically stored in the liver (Dave et al, 1975). We also predicted that the body fat content would be lower in parasitized eels due to energy demands related to hosting the parasite (Khan, 1988;Shanebeck et al, 2022). The great number of individual eels in this dataset (more than 17,000) allowed us to investigate overall effects of parasite presence and intensity on eel condition (mass at a given length).…”