Parasite insight: assessing fitness costs, infection risks and foraging benefits relating to gastrointestinal nematodes in wild mammalian herbivores.

Mammalian herbivores are typically infected by parasitic nematodes, which are acquired through direct, faecal-oral transmission. These parasites can cause significant production losses in domestic livestock, but much less is known about impacts on wild mammalian hosts. We review three elements of parasitism from the host's perspective: fitness costs of infection, risks of infection during foraging and benefits of nutritious pasture. The majority of wildlife studies have been observational, but experimental manipulation is increasing. Treatment with anthelmintics to manipulate parasite load has revealed varied impacts of parasites on fitness variables across host species, but has not produced consistent evidence for parasite-induced anorexia or impaired body condition. Some experimental studies of infection risk have manipulated faecal contamination and detected faecal avoidance by hosts. Only two field studies have explored the trade-off between infection risk and nutritional benefit generated by avoidance of contaminated patches. Overall, field studies of costs, risks and benefits of the host-parasite relationship are limited and few have examined more than one of these elements. Parasitism has much in common with predation, and future insights into anti-parasite responses by wild hosts could be gained from the conceptual and technical developments in research on anti-predator behaviour.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

Anthelmintic Treatment Does Not Change Foraging Strategies of Female Eastern Grey Kangaroos, Macropus giganteus.

Large mammalian herbivores are commonly infected with gastrointestinal helminths. Heavily parasitised hosts are likely to have increased nutritional requirements and would be predicted to increase their food intake to compensate for costs of being parasitised, but experimental tests of the impacts of these parasites on the foraging efficiency of hosts are lacking, particularly in free-ranging wildlife. We conducted a field experiment on a population of free-ranging eastern grey kangaroos (Macropus giganteus) to test this prediction, removing nematodes from one group of adult females using an anthelmintic treatment. We then carried out observations before and following treatment to assess the influence of parasites on foraging behaviour. Contrary to our predictions, the manipulation of parasite burdens did not result in changes in any of the key foraging variables we measured. Our results suggest that despite carrying large burdens of gastrointestinal parasites, the foraging strategy of female kangaroos is likely be driven by factors unrelated to parasitism, and that kangaroos in high nutritional environments may be able acquire sufficient nutrients to offset the costs of parasitism. We conclude that the drivers of forage intake likely differ between domesticated and free-ranging herbivores, and that free-ranging hosts are likely more resilient to parasitism.

Individual heterogeneity and offspring sex affect the growth-reproduction trade-off in a mammal with indeterminate growth.

Reproduction can lead to a trade-off with growth, particularly when individuals reproduce before completing body growth. Kangaroos have indeterminate growth and may always face this trade-off. We combined an experimental manipulation of reproductive effort and multi-year monitoring of a large sample size of marked individuals in two populations of eastern grey kangaroos to test the predictions (1) that reproduction decreases skeletal growth and mass gain and (2) that mass loss leads to reproductive failure. We also tested if sex-allocation strategies influenced these trade-offs. Experimental reproductive suppression revealed negative effects of reproduction on mass gain and leg growth from 1 year to the next. Unmanipulated females, however, showed a positive correlation between number of days lactating and leg growth over periods of 2 years and longer, suggesting that over the long term, reproductive costs were masked by individual heterogeneity in resource acquisition. Mass gain was necessary for reproductive success the subsequent year. Although mothers of daughters generally lost more mass than females nursing sons, mothers in poor condition experienced greater mass gain and arm growth if they had daughters than if they had sons. The strong links between individual mass changes and reproduction suggest that reproductive tactics are strongly resource-dependent.

Experimental manipulation reveals few subclinical impacts of a parasite community in juvenile kangaroos.

Large mammalian herbivores are commonly infected with gastrointestinal helminths. In many host species, these helminths cause clinical disease and may trigger conspicuous mortality events. However, they may also have subclinical impacts, reducing fitness as well as causing complex changes to host growth patterns and body condition. Theoretically, juveniles should experience significantly greater costs from parasites, being immunologically naive and undergoing a significant growth phase. The aims of our study were to quantify the subclinical effects of helminths in juvenile eastern grey kangaroos (Macropus giganteus), which commonly harbour large burdens of gastrointestinal nematodes and are susceptible to associated mass mortality during cold, wet conditions. We conducted a field experiment on a population of free-ranging kangaroos, removing nematodes from one group of juveniles using an anthelmintic treatment. We then compared growth parameters (body condition and growth rates) and haematological parameters of this group with an age-matched, parasitised (untreated) control group. Treated juvenile kangaroos had significantly higher levels of plasma protein (albumin) but, contrary to our predictions, showed negligible changes in all the other parameters measured. Our results suggest that juvenile kangaroos are largely unaffected by their gastrointestinal helminth burdens, and may be able to compensate for the costs of parasites.

Hopping Down the Main Street: Eastern Grey Kangaroos at Home in an Urban Matrix.

Most urban mammals are small. However, one of the largest marsupials, the Eastern Grey Kangaroo Macropus giganteus, occurs in some urban areas. In 2007, we embarked on a longitudinal study of this species in the seaside town of Anglesea in southern Victoria, Australia. We have captured and tagged 360 individuals to date, fitting each adult with a collar displaying its name. We have monitored survival, reproduction and movements by resighting, recapture and radio-tracking, augmented by citizen science reports of collared individuals. Kangaroos occurred throughout the town, but the golf course formed the nucleus of this urban population. The course supported a high density of kangaroos (2-5/ha), and approximately half of them were tagged. Total counts of kangaroos on the golf course were highest in summer, at the peak of the mating season, and lowest in winter, when many males but not females left the course. Almost all tagged adult females were sedentary, using only part of the golf course and adjacent native vegetation and residential blocks. In contrast, during the non-mating season (autumn and winter), many tagged adult males ranged widely across the town in a mix of native vegetation remnants, recreation reserves, vacant blocks, commercial properties and residential gardens. Annual fecundity of tagged females was generally high (≥70%), but survival of tagged juveniles was low (54%). We could not determine the cause of death of most juveniles. Vehicles were the major (47%) cause of mortality of tagged adults. Road-kills were concentrated (74%) in autumn and winter, and were heavily male biased: half of all tagged males died on roads compared with only 20% of tagged females. We predict that this novel and potent mortality factor will have profound, long-term impacts on the demography and behavior of the urban kangaroo population at Anglesea.

The efficacy of anthelmintic drugs against nematodes infecting free-ranging eastern grey kangaroos, Macropus giganteus.

Effective anthelmintics are valuable tools for biologists conducting manipulative field experiments to examine effects of parasites on wildlife. However, before such experiments are carried out the efficacy of these drugs must be determined. We conducted three field experiments (May 2010-September 2011) on free-ranging eastern grey kangaroos (Macropus giganteus) at a golf course in Victoria, Australia, treating animals with the anthelmintic drugs moxidectin (subcutaneous, 1 mg/kg, 2 mg/kg), ivermectin (subcutaneous, 200 µg/kg), and albendazole (oral, 3.8 mg/kg). After treatment we monitored strongylid fecal egg counts (FECs) over time and assessed anthelmintic efficacy using fecal egg count reduction tests (FECRTs). We also performed a larval development assay (LDA) to evaluate directly the efficacy in the nematode population. Unexpectedly, moxidectin and ivermectin had low efficacy with maximum FEC reductions of 82% and 28%, respectively. However, treatment with albendazole reduced FECs by 100% in all kangaroos and egg counts remained low for up to 3 mo. The results from the LDA supported the FECRTs, with low macrocyclic lactone efficacy and high albendazole efficacy. Macrocyclic lactones, at recommended dose rates, were much less effective against strongylid nematodes in kangaroos than has been reported for domestic herbivores. This may be partly due to pharmacokinetics in the host and partly due to low susceptibility in some of the nematodes infecting eastern grey kangaroos.

Experimental manipulation of fertility reveals potential lactation costs in a free-ranging marsupial.

Lactation is the most energetically expensive component of reproduction in mammals. Theory predicts that reproducing females will adjust their behaviour to compensate for increased nutritional demands. However, experimental tests are required, since comparisons of the behaviour of naturally reproducing and non-reproducing females cannot distinguish between true costs of reproduction, individual differences or seasonal variation. We experimentally manipulated reproduction in free-ranging, eastern grey kangaroos (Macropus giganteus), using a fertility control agent. Our novel field experiment revealed that females altered their behaviour in direct response to the energetic demands of reproduction: reproducing females increased bite rates, and thus food intake, when the energetic demands of lactation were highest. Reproducing females did not reduce the time spent on vigilance for predators, but increased their forage intake on faecal-contaminated pasture, thereby increasing the risk of infection by gastrointestinal parasites-a largely unrecognized potential cost of reproduction.