Abstract

BackgroundThe study of changes in a host’s energy allocation in response to parasites is crucial for understanding parasite impact on both individual- and population-level processes. Experimental studies have explored such responses mainly in a single subsample of hosts per study, primarily adult males, and have only assessed either the overall energy acquisition or expenditure, rather than their different components simultaneously, or the behavioral responses. Accordingly, two fundamental questions arise: why have multiple host strategies evolved to cope with increased energy expenditure? and, which factors determine this variation (e.g. host species, identity, age)? This study provides an important step towards addressing both questions by experimentally disentangling the short-term physiological and behavioral responses of juvenile and non-reproductive adult rodents to natural levels of flea infestation. These two cohorts represent extreme cases of the energy demand continuum, as the former, in contrast to the latter, is involved in growth - a highly energy-demanding process - and may not be able to operate far below its upper limit of energy expenditure, and thus should reduce its energy expenses upon the occurrence of extra demands (e.g. due to parasitic pressure). Accordingly, we hypothesized that the response to fleas is age-dependent and varies according to the age-specific energy requirements and constraints.MethodsWe monitored the behavior and physiology of juvenile and non-reproductive adult rodents before and after experimental flea infestation. First, we used a model selection approach to search for the factors that best explained the variability in the time budget, oxygen consumption, and body mass change in response to fleas. Then, using a path analysis approach, we quantified the different pathways connecting the important associations revealed at stage 1.ResultsCompared to their flea-free counterparts, flea-infested adults groomed longer and had a higher oxygen consumption rate, but did not lose body mass. Infested juveniles also groomed longer but grew slower and had a similar rate of oxygen consumption.ConclusionsResults suggest that both juvenile and adult rodents suffer from natural flea infestation levels. However, the comparison between the responses of juveniles and adults to experimental infestation, also suggests that juveniles may reallocate their energy expenditure from growth to maintenance, while non-reproductive adults increase their energy acquisition. Such age-dependent responses suggest that juveniles may be constrained by their higher need to rest for full functioning or by an upper limit in energy expenditure. Taken together, our study provides experimental evidence that hosts can compensate for the costs incurred by parasitism through physiological and behavioral plasticity, depending on their age, which probably determines their requirements and constraints. These compensatory responses may have important implications for the population dynamics of hosts and their parasites.

Highlights

  • The study of changes in a host’s energy allocation in response to parasites is crucial for understanding parasite impact on both individual- and population-level processes

  • Garrido et al Parasites & Vectors (2016) 9:120 (Continued from previous page). Results suggest that both juvenile and adult rodents suffer from natural flea infestation levels

  • The comparison between the responses of juveniles and adults to experimental infestation, suggests that juveniles may reallocate their energy expenditure from growth to maintenance, while non-reproductive adults increase their energy acquisition. Such age-dependent responses suggest that juveniles may be constrained by their higher need to rest for full functioning or by an upper limit in energy expenditure

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Summary

Introduction

The study of changes in a host’s energy allocation in response to parasites is crucial for understanding parasite impact on both individual- and population-level processes. This study provides an important step towards addressing both questions by experimentally disentangling the short-term physiological and behavioral responses of juvenile and nonreproductive adult rodents to natural levels of flea infestation These two cohorts represent extreme cases of the energy demand continuum, as the former, in contrast to the latter, is involved in growth - a highly energydemanding process - and may not be able to operate far below its upper limit of energy expenditure, and should reduce its energy expenses upon the occurrence of extra demands (e.g. due to parasitic pressure). Energy acquisition is a function of both the availability and quality of food consumed and of the rate and efficiency of food collection and digestion (Fig. 1) This acquired energy is used for maintenance, thermoregulation, and activity, and for tissue production and biological processes, such as growth, reproduction, fat storage, and immunity (Fig. 1). Since an energy shortage for maintenance often results in irreversible damage, the host must compensate for the negative impact of parasites by changing its available energy allocation

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