situation, uninfected animals were most effective at parasite avoidance as they consumed fewer parasite larvae relative to what was available on pasture. q 2000 Elsevier Science B.V. All rights
reserved.
Keywords: Sheep; Feeding and nutrition; Foraging behaviour; Grazing behaviour; Parasitism; Spatial distribu- tion
1. Introduction
The need to avoid parasites acts as a major selection pressure in the evolution of Ž
. Ž
. animal behaviour Hart, 1990 . Elements of migratory Folstad et al., 1991 , social
Ž .
Ž .
Ž .
Loehle, 1995 , sexual Kavaliers and Colwell, 1995b and grooming Mooring 1995 behaviours of hosts all play a role as parasite defence strategies. Surprisingly, there have
been few studies that investigate the role that an animal’s foraging strategy can play in behavioural defence against parasites. It has been established that negative factors such
Ž .
Ž .
as the risk of predation Edwards, 1983 , competition Millikan et al., 1985 and Ž
. consuming plant toxins Provenza et al., 1998 can have a constraining influence on a
herbivore’s foraging strategy. Foraging animals should also be constrained by the risk of Ž
. parasite infection Lozano, 1991 . Recent studies suggest that this is indeed the case
Ž .
Hutchings et al., 1998, 1999 , although further evidence is required. Gastrointestinal parasites can have detrimental effects on the fitness of an animal
Ž .
Hart, 1990 . For example, when animals are under nutritional stress, gastrointestinal helminths may increase in number within the host and can be a contributing factor in
Ž .
host mortality Hart, 1990; Gulland, 1992 . Parasites can also incur a less apparent cost to host fitness by having detrimental effects on the location of resources and spatial
Ž learning, reproduction, predator avoidance and territorial defence Godin and Sproul,
1988; Milinski, 1990; Moore and Gotelli, 1990; Zuk, 1992; Moller et al., 1993; .
Kavaliers and Colwell 1995a . Hence, minimising the number of parasites which are ingested whilst foraging should be a driving force in shaping foraging strategies.
Ž Ruminants are known to avoid grazing herbage which is contaminated with faeces e.g.
. Gruner and Sauve, 1982; Hutchings et al., 1998, 1999 . Foraging in close proximity to
faeces carries a risk of parasite infection as such areas are reservoirs of gastrointestinal Ž
. parasite larvae Williams and Bilkovich, 1973 . Consequently, it has long been thought
that avoidance of contaminated swards by ruminants might be a parasite defence strategy.
It is not clear which cues a grazing animal uses when discriminating against faeces-contaminated herbage. There is evidence that animals can distinguish between
Ž .
uninfected and infected individuals Kavaliers and Colwell, 1995b and also between Ž
. faeces from uninfected and infected animals Evans et al., 1992; Pappas et al., 1995 ,
presumably by olfactory means. Consequently, in the current study the role of three Ž
possible cues faeces from parasite-free sheep, faeces from parasite-infected sheep, and .
parasite larvae alone in the detection of contaminated patches of pasture were investi- gated.
If avoidance of faecally contaminated herbage is a parasite defence strategy, it must Ž
. be effective in helping an animal to avoid or remove parasites Hart, 1990 . However,
only one previous study has experimentally examined whether avoidance of faeces by Ž
. ruminants results in a reduction in the number of parasites consumed. Michel 1955
compared the number of Dictyocaulus ÕiÕiparus larvae isolated from herbage immedi- ately adjacent to where cattle grazed with the number isolated from random samples of
pasture herbage. He concluded that cattle grazed in a manner that resulted in the consumption of fewer larvae than if grazing was random and that selective grazing was
a parasite avoidance strategy. However, this conclusion was based only on estimates of the numbers of larvae that cattle ingested. In the study reported here we used direct
measurements of consumed parasite larvae to lend weight to our findings.
Environmental and internal factors, other than simply the presence of faeces on herbage, may affect the ability of ruminants to distinguish between clean and contami-
nated areas. Selection of alternate foods by sheep is known to be influenced by the scale Ž
. of aggregation of patches Edwards et al., 1994 . Hence, in this study the influence of
the scale of aggregation of faeces-contaminated patches had on diet selection was investigated. Factors, internal to the animal, which play a part in diet selection include
Ž .
parasitism. Hutchings et al. 1998, 1999 conducted a series of small-scale diet-choice experiments and observed that parasite-infected sheep avoid faeces contaminated swards
more than uninfected sheep. Although demonstrative, these studies were conducted in artificial conditions. The current study approaches more natural conditions, as the effect
of parasite infection on faeces avoidance behaviour by sheep on pasture was investi- gated.
This paper presents two experiments, the aims of which were to investigate the cues used by sheep to avoid faecal contaminated patches, how avoidance of faecal-contamina-
tion and ingestion of parasite larvae by sheep on pasture was influenced by the spatial distribution of contaminated patches, and how parasite infection status influences
grazing by animals.
2. Materials and methods
