Flea infestation, social contact, and stress in a gregarious rodent species: minimizing the potential parasitic costs of group-living.

Both parasitism and social contact are common sources of stress that many gregarious species encounter in nature. Upon encountering such stressors, individuals secrete glucocorticoids and although short-term elevation of glucocorticoids is adaptive, long-term increases are correlated with higher mortality and deleterious reproductive effects. Here, we used an experimental host-parasite system, social rodents Acomys cahirinus and their characteristic fleas Parapulex chephrenis, in a fully-crossed design to test the effects of social contact and parasitism on stress during pregnancy. By analysing faecal glucocorticoid metabolites, we found that social hierarchy did not have a significant effect on glucocorticoid concentration. Rather, solitary females had significantly higher glucocorticoid levels than females housed in pairs. We found a significant interaction between the stressors of parasitism and social contact with solitary, uninfested females having the highest faecal glucocorticoid metabolite levels suggesting that both social contact and infestation mitigate allostatic load in pregnant rodents. Therefore, the increased risk of infestation that accompanies group-living could be outweighed by positive aspects of social contact within A. cahirinus colonies in nature.

Subtle short-term physiological costs of an experimental augmentation of fleas in wild Columbian ground squirrels.

Parasites affect many aspects of host physiology and behavior, and thus are generally thought to negatively impact host fitness. However, changes in form of short-term parasite effects on host physiological markers have generally been overlooked in favor of fitness measures. Here, we studied flea (Oropsylla idahoensis and Oropsylla opisocroistis tuberculata) parasitism on a natural population of Columbian ground squirrels (Urocitellus columbianus) in Sheep River Provincial Park, AB, Canada. Fleas were experimentally added to adult female U. columbianus at physiologically demanding times, including birth, lactation and weaning of their young. The body mass of adult females, as well as their oxidative stress and immunity were recorded multiple times over the active season under flea-augmented and control conditions. We also measured the prevalence of an internal parasite (Trypanosoma otospermophili). Doubly labeled water (DLW) was intra-peritoneally injected at peak lactation to examine energy expenditure. Effects of parasites on oxidative stress were only observed after offspring were weaned. There was no direct effect of experimentally heightened flea prevalence on energy use. A short-term 24 h mass loss (-17 g) was detected briefly after parasite addition, likely due to U. columbianus preferentially allocating time for grooming. Our parasite augmentation did not strongly affect hosts and suggested that short-term physiological effects were unlikely to culminate in long-term fitness consequences. Columbian ground squirrels appear to rapidly manage parasite costs, probably through grooming.

Energy expenditure for egg production in arthropod ectoparasites: the effect of host species.

We studied the energy cost of egg production in two flea species (Parapulex chephrenis and Xenopsylla ramesis) feeding on principal (Acomys cahirinus and Meriones crassus, respectively) and auxiliary (M. crassus and A. cahirinus, respectively) rodent hosts. We predicted that fleas feeding on principal as compared with auxiliary hosts will (a) expend less energy for egg production; (b) produce larger eggs and (c) live longer after oviposition. Both fleas produced more eggs and spent less energy per egg when exploiting principal hosts. Parapulex chephrenis produced larger eggs after exploiting auxiliary hosts, while the opposite was true for X. ramesis. After oviposition, P. chephrenis fed on the auxiliary hosts survived for a shorter time than those fed on the principal hosts, while in X. ramesis the survival time did not differ among hosts. Our results suggested that one of the proximate causes for lower reproductive performance and subsequent lower abundance of fleas on auxiliary hosts is the higher energy cost of egg production. However, in some species, lower offspring number may be compensated to some extent by their size, although this compensation may also compromise their future reproduction via decreased survival. In addition, the reproductive strategy of exploitation of low profitable (i.e. auxiliary) hosts may differ between flea species.

Driven to distraction: detecting the hidden costs of flea parasitism through foraging behaviour in gerbils.

Gerbilline rodents such as Allenby's gerbils (Gerbillus andersoni allenbyi), when parasitized by fleas such as Synosternus cleopatrae pyramidis, devote long hours of grooming to remove the ectoparasites. Yet no detrimental energetic or immunological effects of the ectoparasites have been found in adult Allenby's gerbil. Why should gerbils go to such trouble? We tested for the various ways that fleas can negatively affect gerbils by manipulating flea infestation on gerbils and the presence of a fox. We demonstrate that gerbils responded to fleas by leaving resource patches at higher giving-up densities. Furthermore, they stayed in those resource patches less time and left them at higher quitting harvest rates so long as a fox was also present. When flea-ridden, gerbils also abandoned using vigilance to manage risk and relied mainly on time allocation. Thus, having fleas imposed a foraging cost similar in nature to that arising from the risk of predation from foxes and may be even larger in magnitude. More than that, the presence of fleas acted as a magnifier of foraging costs, especially those arising from the risk of predation. The fleas reduced the gerbils' foraging aptitude and altered how they went about managing risk of predation. We hypothesize that fleas reduce the attention that gerbils otherwise have for foraging and predator detection. We suggest that this is the major cost of ectoparasitism.

Costs and benefits of experimentally induced changes in the allocation of growth versus immune function under differential exposure to ectoparasites.

BACKGROUND: Ecological immunology has focused on the costs of investment in immunocompetence. However, understanding optimal resource allocation to immune defence requires also identification of its benefits, which are likely to occur only when parasites are abundant. METHODOLOGY: We manipulated the abundance of parasitic hen fleas in blue tit (Cyanistes caeruleus) nests, and supplemented their hosts, the nestlings, with methionine (a sulphur amino acid enhancing cell-mediated immunity) during day 3-6. We found a significant interaction between these two experimental factors on the development of immune defences and growth rates. Only in parasitized nests did methionine supplementation boost immune (PHA) response, and did nestling with experimentally increased immunocompetence show a relatively faster growth rate than control nestlings between days 6-9. Hence, the allocation of resources into immune defence and its growth-benefits are apparent only in presence of parasites. The main cost of methionine-induced increased allocation to the immune system was an increase in mortality, independently of ectoparasites. Nestlings in all treatments compensated initial growth reduction and all reached equal body size at day 16 (just prior to fledging), indicating a lack of long-term benefits. In addition, methionine treatment tended (P = 0.09) to lower circulating plasma immunoglobulin levels, possibly indicating a trade-off between the cell-mediated and humoral components of the immune system. CONCLUSIONS: We found no strong benefits of an increased investment in immunocompetence in a parasite-rich environment. Any deviation from the growth trajectory (due to changes in allocation induced by methionine) is largely detrimental for survival. Hence, while costs are apparent identifying the benefits of investment in immunocompetence during ontogeny is challenging.

Morbidity assessment in sand flea disease (tungiasis).

Tungiasis, caused by the sand flea Tunga penetrans, is a health problem in many impoverished communities in Latin America, the Caribbean, and sub-Saharan Africa. Sand flea disease is associated with a broad spectrum of clinical and histological pathology. The factors determining the disease burden in endemic communities are not well understood, and severity of clinical pathology has never been assessed quantitatively. Thus, two severity scores were developed: one for acute disease and one for chronic sequels. These scores were evaluated in a cohort of 70 severely infested patients living in a shantytown in Fortaleza, a capital city in Northeast Brazil. Patients were examined during a period of 25 days and followed-up after a twice daily application of a plant-based repellent to prevent reinfestation. The severity score for acute disease symptoms significantly correlated with the infestation rate and the number of embedded fleas. It turned zero when reinfestation was prevented. The score for chronic disease also significantly correlated with the infestation rate. Tungiasis is associated with considerable acute and chronic morbidity. The degree of acute morbidity is directly related to the number of embedded sand fleas. When transmission is interrupted, the chronic morbidity reflects the infestation rates individuals have experienced in the past.

Energy costs of blood digestion in a host-specific haematophagous parasite.

Fleas consume and digest blood from their hosts. We hypothesized that the energy costs of digestion of blood by fleas is dependent on the host species. To test this hypothesis, we studied CO2 emission, a measure of energy expenditure, during digestion of a blood meal taken by Parapulex chephrenis from a preferred (Acomys cahirinus) and a non-preferred (Gerbillus dasyurus) host. We predicted that the energy cost of digestion would be lower for A. cahirinus blood than that for G. dasyurus. Male and female fleas consumed similar amounts of blood per unit body mass, independent of host species. Our prediction was supported in that fleas expended significantly more energy digesting blood of G. dasyurus than blood of A. cahirinus. We also found CO2 emission rates of fed fleas were higher than those of unfed fleas and differed significantly among stages of blood digestion when a flea fed on G. dasyurus but not when it fed on A. cahirinus. When fed on G. dasyurus, fleas spent less energy during earlier than later stages of digestion.