Time budget, oxygen consumption and body mass responses to parasites in juvenile and adult wild rodents

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.

Ectoparasite‐induced increase in Drosophila host metabolic rate

“…This suggests larger parasites infecting smaller hosts may have a larger effect on metabolism, as is the case in the Drosophila ‐ Macrocheles system and the isopod‐bream system. However, other studies have failed to detect a significant effect or the full magnitude of parasitism on host respiration; and this may be because they only considered parasite presence/absence or a single level of infection (Careau et al, 2010; Garrido et al, 2016; Gudowska et al, 2016; Filipsson et al, 2017; Luong et al, 2017b). Therefore, future studies should examine the consequences of a range of infection intensities on host metabolism, as done here and in other studies (Giorgi et al, 2001; Careau, Thomas and Humphries, 2010; Moretti et al, 2017).…”

“…Therefore, future studies should examine the consequences of a range of infection intensities on host metabolism, as done here and in other studies (Giorgi et al, 2001; Careau, Thomas and Humphries, 2010; Moretti et al, 2017). Another limitation of previous studies that needs to be remedied is the convention of measuring respiratory rates at a single time point, usually, after an infection has established (Khokhlova et al, 2002; Garrido et al, 2016; Chodkowski and Bernot, 2017; Luong, Horn, and Brophy, 2017). These previous studies only provide a snapshot in time, whereas our study highlights the value of using a before‐and‐after design as it controls for pre‐existing biases and offers clear evidence of a causal relationship between parasitism and increased host metabolism.…”

Assessing functional redundancy in Eurasian small mammal assemblages across multiple traits and biogeographic extents

“…Host activity can influence parasite sharing, altering host–parasite networks (Reece et al 2017, Dallas et al 2019), by processes such as circadian rhythms of the host's immune system or couplings between parasite transmission and host activity cycles (Reece et al 2017) . Conversely, parasitic infections directly alter activity patterns (Flowerdew 2000), and may induce anti‐parasitic behaviors (Stanko et al 2002, Garrido et al 2016) which indirectly modify activity patterns (Wauters 2000).…”

A Potential Role for mu-Opioids in Mediating the Positive Effects of Gratitude

“…The principle effect of primate allogrooming appears to be the maintenance of harmonious societies (Russell and Phelps, 2013); primate social groups tend to be larger than those of other animals, and their social relationships tend to be more complex, diverse, and long lasting (Machin and Dunbar, 2011). Allogrooming settles in-group tensions, maintains social bonds, reinforces social hierarchies, and provokes reciprocal prosocial behavior in the form of reciprocal grooming, food sharing, or coalitionary support (de Waal, 1997; Akinyi et al, 2013; Jaeggi and Gurven, 2013; Lutermann et al, 2013; Borgeaud and Bshary, 2015; Garrido et al, 2016; Richard et al, 2016). The parallels between the effects of allogrooming and the effects of gratitude on social behavior are apparent, and a possible link between the social effects of allogrooming and physiology emerges from the observation that when an individual is being groomed, they visibly relax and their heart rate decreases significantly (Grandi and Ishida, 2015).…”