Do parasitism and nutritional status interact to affect production in snowshoe hares?

Ecology, June, 1998 by Dennis L. Murray, Lloyd B. Keith, John R. Cary

INTRODUCTION

Nutritional status of animals is affected proximally by the energy that is stored from food, which is related both to food quality and quantity and the efficiency of digestion. Energy available for production (growth, storage, and reproduction) consists of the difference between metabolizable energy and the energy used for body maintenance (Karasov 1986); adequate nutrition typically results in greater production than does poor nutrition (Robbins 1993).

Parasitism can influence nutritional status by directly affecting host physiology and behavior (Hall 1985, Yuill 1987, Scott 1988). Accordingly, some parasites appropriate significant amounts of nutrients from hosts resulting in marked reductions in energy uptake (Schall et al. 1982, Connors and Nickol 1991, Moller et al. 1994), but other parasites appear to cause little or no effect on host energetics (Bailey 1975, Munger and Karasov 1989, 1994). Clearly, animal body condition and reproductive status should be compromised when parasites inflict substantial energetic costs (e.g., Hudson 1986, Korpimaki et al. 1993, Moller 1993, Richner et al. 1993, Tocque 1993). However, parasites do not necessarily induce negative effects if hosts have an energy surplus concurrent with the infection (Munger and Karasov 1989), are able to compensate for losses through increased food acquisition (Moller 1994, Tripet and Richner 1997), or can mitigate reduced condition by adaptively regulating investment into production (Forbes 1993). This suggests that the outcome of host parasite associations may be contingent on host nutritional status as well as severity of infection, both of which can be influenced by factors that are largely extrinsic to the host-parasite relationship (Holmes and Price 1986, Minchella and Scott 1991).

Host malnutrition may adversely affect resistance to parasitic infection by reducing the efficacy of the immune system (Bundy and Golden 1987, Burkolder and Swecker 1990, Crompton 1991, Solomons and Scott 1994). Food shortage could thereby result in higher parasite burden, which in turn may increase nutritional demands on the host and accentuate effects of food shortage. Thus, the relationship between nutritional status and parasitism is allegedly synergistic, and the individual effects of each factor on host nutritional status can be amplified, when co-occurring. The interaction between host nutrition and parasite immunity has been explored in several laboratory studies (Crompton et al. 1981, Keymer et al. 1983, Crompton et al. 1985, Slater and Keymer 1986), leading to the speculation that natural vertebrate populations may be influenced by interactive effects of food shortage and parasitism (e.g., Laine and Henttonen 1983, Mihok et al. 1985, Keymer and Dobson 1987, Holmes 1995). Although numerous manipulations of animal nutrition (i.e., food supplementation experiments) have been undertaken in the field (see review by Boutin 1990), studies examining potential interactive effects of food and parasitism have not been attempted. However, because subtle effects of parasitism may be masked by other factors, multifactorial experiments are necessary to effectively assess the possible indirect role of parasites in the field (Minchella and Scott 1991).

To explore the possibility that nutrition and parasitism are synergistic in free-ranging vertebrates, we increased food supplies and decreased nematode numbers in a naturally infected snowshoe hare (Lepus americanus) population, and assessed the direct and interactive effects of manipulations on hare production. We hypothesized that nutrition and parasitism would act synergistically on hare production and that animals subjected to both treatments should have (1) lower parasite burdens, and (2) higher production (as measured by body mass, fat reserves, and fecundity) than animals experiencing only one or no treatments. We predicted that the benefits of parasite reduction and food supplementation in hares receiving both treatments should be multiplicative, not additive. We also considered an alternative possibility that parasites and food did not influence hare production, or did so independently of each other.

METHODS

Study site

The experiment was conducted on the Narcisse Wildlife Management Area, in southcentral Manitoba, Canada (51 [degrees] N, 98 [degrees] W), between April 1991 and June 1993. The study site was a 15- to 40-yr-old aspen (Populus tremuloides) forest with an understory of several species of deciduous shrubs. Hare populations have, historically, been strongly cyclic within Manitoba (Keith and Rusch 1988), and on our site (Rusch et al. 1978). Throughout the study, average hare densities on food-normal (unsupplemented) areas (0.3-0.4 hares per hectare; D. L. Murray, unpublished data) were lower than most other hare populations studied across North America (three to nine hares per hectare; see review by Keith 1990). The cyclic crash of other hare populations across the continent one year prior to the onset of our study (e.g., Boutin et al. 1995), lead us to infer that our study coincided with a cyclic low in the local population.