Spatial learning and discrimination of food patches in the European badger (Meles meles L.)

Anirn. Behav., 1986, 34, 1129 1134

Spatial learning and discrimination of food patches in the European badger (Meles meles L.) R. L. M E L L G R E N * & T. J. ROPERt:~

*Department of Psychology, University of Oklahoma, Norman, OK 73019, U.S.A. ~School of Biology, University of Sussex, Brighton BN1 9QG, Sussex, U.K.

Abstract. Theories of foraging often assume that concentrations of prey ('patches') can be discriminated by a forager, but there have been few studies of how this is achieved when patches are not recognizable by means of an obvious proximal cue. We observed the search trajectories of two badgers (Meles meles L.) foraging for peanuts in artificial patches to see how efficiently they could map a new patch in the first place, and whether they would remember the location and extent of a previously visited patch. The results suggest that when a patch is encountered for the first time, a strategy of area-restricted searching keeps the animal's trajectory largely within the patch boundary. After a single exposure to a novel patch, however, badgers show evidence of being able to remember its location and extent, apparently with reference to distal landmarks.

In natural environments, food or other resources are often distributed in clumps or 'patches' of relatively high abundance against a background of relatively low abundance (e.g.C.J. Krebs 1978). For a bee, for example, a patch might be an inflorescence loaded with nectar (e.g. Pyke 1981); for a wagtail it might be a cowpat that has attracted a concentration of dungffies (e.g. Davies 1977). There have been numerous theoretical and empirical studies of the way in which a predator distributes its time between patches differing in prey density (see reviews by J. R. Krebs 1978; Krebs & McCleery 1984), but comparatively little attention has been given to the problem of how a predator might gain information about patch location in the first place (Zach & Falls 1976; Bond 1980). In many cases the problem of patch localization is trivial because some aspect of the prey or its residence is detectable from a distance. For example a bee can easily recognize the location and extent of a patch of nectar because the nectar is contained in a conspicuous inflorescence; a great tit can recognize that a fir cone constitutes a likely patch of insect larvae (e.g. Cowie 1977). In other cases, however, there is no obvious cue distinguishing a patch from the surrounding environment, and it is with the localization of such 'hidden' food patches that the present paper is concerned. An everyday example of a hidden patch would be a local concentration of worms within one particular $ To whom all correspondence should be addressed.

part of a lawn: the patch is hidden in that the lawn appears uniform to a bird foraging on the surface (Smith 1974). The purpose of our experiment was to examine the ability of the European badger (Meles meles L.) to locate and remember the extent of hidden food patches in field conditions. In natural circumstances, badgers feed mainly on worms and other invertebrates (e.g. Neal 1977; Kruuk & Parish 1981), and there is reason to suppose both that worms are patchily distributed (Smith 1974; Kruuk & Parish 1982) and that badgers are sensitive to spatial differences in worm availability (Kruuk & Parish 1982). Badgers are also quick to take advantage of new food sources such as compost heaps, garden vegetables and agricultural crops (Harris 1982). There is thus evidence that badgers are natural patch foragers and also that they readily adapt their behaviour to changes in prey distribution and abundance. In our experiments, food (shelled peanuts) was provided in artificial 'patches' of fixed location during a series of trials, and the ability of wild badgers to restrict their foraging efforts to the patches was assessed. Test trials were run to see whether animals remembered the locution of previous patches. Results from two animals suggest that on their first encounter with a novel patch, badgers are able to track the patch boundary to an impressive degree. The results also suggest that badgers can remember the location and extent of a new patch after only one trial.

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Study Area and Subjects

The study was conducted in an area of private farmland in the south of England, consisting of a mixture of rough pasture, arable crops and scrub (see Roper et al., in press, for further details). The experimental animals were two adult badgers, a male weighing 8-2 kg and a female weighing 9'0 kg. They were members of a social group containing an estimated nine individuals, which was the focus of a long-term study of badger social behaviour and ecology. In the course of this study, both experimental animals, and several other members of the same social group, had been live-trapped, weighed and fitted with radio-collars so that they could be identified individually. In addition, a small fluorescent green 'betalight' (Saunders-Roe Ltd) was fitted to the top of each radio-collar, enabling an animal to be located in the dark at distances of up to 75 m with the naked eye, or up to 200 m with binoculars.

Procedure

We recorded the search trajectories of two radiocollared badgers hunting for peanuts in three adjacent 50-m 2 areas (patches) located along a fenceline about 120 m from the animals' home sett. The field in which the experimental patches were set up consisted of rough pasture occasionally grazed by cattle, and the area chosen for the patches was one which badgers often passed through and where they occasionally foraged for worms. The three adjacent patches are referred to as patches A, B and C (see Fig. 1). The patches were baited with shelled peanuts at about 1900 hours G M T on successive evenings, and the badgers emerged from the sett and visited the patches (once they had discovered their existence) from about 2000 hours G M T onwards. The badgers were viewed from a hillside above the experimental area using 7 x 50 binoculars and a red-filtered 15-W tungsten-halogen spotlight, from a distance of 55 m. The animals' movements were recorded verbally on a dictaphone, using the fenceposts and other topographical features (e.g. clumps of grass) as reference points. Additional reference points were provided by small wooden stakes at the corner of each patch. On most occasions, the

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5m Figure 1. Layout of the three artificial food patches A, B and C during (a,b) training trials and (c) test trials. Dotted lines indicate the notional patch boundaries; the solid line running along the north (top) edge of the patches denotes a fence; open circles denote fence-posts; filled circles denote piles of peanuts. The observers sat on a hillside overlooking the area from the south side; the home sett from which the animals emerged was to the east.

animals visited the experimental patches while it was still light but, even after dusk, visibility was sufficient to allow detailed recording of search paths and to identify and time individual prey 'captures'. Search trajectories were reconstructed the next day from the tape-recorded observations. On two occasions both observers (RLM and TJR) simultaneously recorded the same search path, and the transcribed paths were compared as a check on observer reliability. Agreement was found to be good. The experiment consisted of a number of training trials in which only certain patches were baited, followed by test trials in which all patches were baited. The idea was to see (a) how good the badgers would be at learning the initial distribution of food, and (b) whether knowledge of the distribution of food during training would influence behaviour during test trials. For badger 1, the procedure was as follows. During trials 1-6, patches A and C only were baited

Mellgren & Roper." Spatial discrimination by badgers with eight piles of peanuts spaced out in a regular manner, as shown in Fig. 1a. Some piles contained 3 nuts and others 15 nuts, but there was no evidence that the badgers responded differently to the two sizes of 'prey' and so this aspect of the design is irrelevant. During trial 7 (test trial), a single pile of 15 peanuts was placed in the centre of each of patches A, B and C, as shown in Fig. lc, There then followed a single retraining trial (trial 8) in which eight piles of peanuts were placed in patch B only (Fig. lb); and a further test trial in which a single pile of peanuts was placed in the centre of each of patches A, B and C (Fig. lc). On the day after each trial the patches were inspected and any uneaten peanuts were recovered. For badger 2 the training sequence was reversed. In trials 1-6, patch B only was baited with eight piles of peanuts; in trial 7 (test trial) all three patches were baited with a single pile; in trial 8 (retraining) patches A and C only were baited with eight piles; in trial 9 (test trial) all three patches were baited with a single pile. Badger 1 was tested during summer 1984, badger 2 during spring 1985. Other animals from the same sett sometimes visited the patches, but results are

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reported only from the two animals on which it proved possible to conduct a full series of trials. Different individuals usually visited the patches at different times of night, and on only two occasions was it necessary to abandon a trial because of interference from another animal. On both occasions the trial was re-run the next night.

RESULTS

Training Trials The first aim of the experiment was to see whether the foraging efficiency of badgers would improve with repeated exposure to a particular pattern of food distribution. In fact, both badgers responded efficiently during the first trial in which they encountered the experimental patches: that is, badger 1 searched intensively in patches A and C (the baited patches) and more or less ignored patch B (unbaited), while badger 2 searched intensively in patch B and more or less ignored patches A and C (see Fig. 2a). By trial 6 (Fig. 2b) the search paths had become even more efficient, in the sense that

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Figure 2. Search paths for each individual badger in trials 1, 6, 7 and 9. Patch boundaries are demarcated by a broken line except along the north (top) edge where a solid line denotes the boundary fence.

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Table I. Time spent searching (s) for each badger in each of patches A, B and C, and total search time in all three patches, for trials 1 and 6 (training) and 7 and 9 (testing) Badger 1 Trial 1 6 7 9

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Total 520 330 290 580

** Patches that were baited with eight piles of peanuts; * patches baited with a single pile of peanuts; unbaited patches have no asterisk.

relatively less time was spent in the unbaited patches. Table I shows the time spent by each badger in each patch, and the total foraging time, for trials 1 and 6. Timing started when an animal entered a patch for the first time, and ended either when the animal had consumed all the bait or when it left the area for at least 2 rain. On most trials animals found and devoured all available peanuts before leaving, In calculating the time spent in each patch, the clock was stopped while an animal was standing still consuming peanuts, so that the times given in Table I represent search times. Table I confirms that both animals spent more time searching in baited than in unbaited patches. Total search time decreased between trials 1 and 6, providing further evidence that foraging efficiency improved with experience.

Test Trials

The second aim of the experiment was to see whether badgers would continue, during test trials, to concentrate their search effort in previously baited patches. Figure 2c shows search trajectories for each animal in the first test trial (trial 7), and shows that both animals did concentrate their searching in the previously baited patch or patches (patches A and C for badger 1; patch B for badger 2). The search times given in Table I confirm this result. In trial 8, each animal was given a single experience with the bait distributed in a different pattern from that previously encountered during trials 1-6. Specifically, patch B was baited for

badger 1, and patches A and C for badger 2. Figure 2d shows search trajectories during the subsequent test trial (trial 9), and Table I shows the corresponding search times. Both badgers spent more time searching in the square or squares that had been baited in trial 8 than in the square or squares that had been unbaited in trial 8, despite having had only a single experience of the new pattern of distribution of bait.

DISCUSSION The initial aim of the study was to see how efficiently badgers would utilize a food patch that was completely novel to them and was hidden in the sense that it could not be recognized by obvious proximal cues. Our expectation was that if food was provided in the same place on a number of occasions, the animals would gradually learn the exact location and extent of the baited area. This expectation was confirmed in that there was some improvement in foraging efficiency over the first six training trials. However, a striking feature of the results was the extent to which foraging effort was concentrated within the patch boundaries on the first trial, when the patches were completely novel. One possible explanation of the efficient foraging of naive badgers is that they can locate peanuts from a distance by smell, so that our patches were not hidden from the badger's point of view. However, this seems unlikely: even after several trials the badgers showed no signs of being able to home in on piles of peanuts directly, and often they would pass within inches of peanuts without

Mellgren & Roper: Spatial discrimination by badgers detecting them. Rather they would meander around nuzzling in the grass with their snouts, moving the head from side to side until peanuts were directly contacted with the snout. A more likely explanation of the efficient performance of the badgers on trial 1 is that the animals have an inherent tendency, once they have captured a prey item by chance, to search more thoroughly in the immediate vicinity of the capture, a type of behaviour known as 'area restricted searching' (Tinbergen et al. 1967). Area restricted searching has been demonstrated in various species offish, insects and birds, and can involve changes in a number of parameters of the search path such as rate of movement, average rate of turning, average angle of turn and degree of asymmetry (see reviews by Thomas 1974; Bond 1980). Our observations of badgers foraging for peanuts suggest that they slow down and adopt a more tortuous search path immediately after encountering food, and computer simulations (Shepherdson, in preparation) show that this can have the effect of keeping the animal within a patch whose boundaries are not otherwise detectable. More specifically, data from badgers 1 and 2, in which 182 prey 'captures' were observed, show that immediately after making a capture the animals spent an average of 50.5 s (range 12-100 s) nosing around within the immediate vicinity of that capture (i.e. within a distance of 1 m from the place where the bait had been). This figure excludes time spent actually consuming the bait. In between captures the animals moved relatively linearly (see Fig. 2) at an average speed of 15.4 m/min. Thus our observations suggest that badgers use two distinct foraging modes: a post-capture mode consisting of intense searching within a localized area, accompanied by vigorous snuffling in the grass with the snout and sometimes also by pawing or digging with the front legs; and a pre-capture mode consisting of steady forward motion accompanied by sideto-side movements of the head, with the nose held close to the substrate, as if the animal were attempting to cut a wide olfactory swathe through the area to be searched. Interestingly, when they are hunting for worms, badgers slow down and search more thoroughly immediately after making a capture (Shepherdson, in preparation), and this strategy makes sense since worms are reported to occur in local pockets of dense concentration within a larger patch (Satchell 1983). The second aim of the experiment was to see

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whether badgers could remember the location of previously baited patches. Behaviour in trials 7 and 9 suggests that they can, since previous patterns of searching persisted despite the fact that in these trials all three patches were equally baited, Furthermore, behaviour in trial 9 shows significant retention after just one exposure to a new pattern of bait distribution. One-trial learning of the location of a hidden patch or patches is especially significant since studies of distal localization in rats (e.g. Morris 1981), birds (Zach & Falls 1976) and bees (Cartwright & Collett I983) suggest that it takes an animal many trials to learn the location of a hidden target relative to distal landmarks, even in artificial conditions where the total area to be searched is restricted and where the distance between landmarks and target is at most one or two metres. On the other hand, studies of memory for previously visited flowers in a nectar-eating bird (Kamil 1978) and of memory for locations of stored food in marsh tits (Sherry 1982), suggest the ability to recognize previously visited sites after a single experience. It may be the case, therefore, that studies of distal localization in the laboratory have underestimated the ability of animals to remember the locations of hidden targets. The above discussion assumes that badgers located our food patches with reference to distance landmarks such as bushes, trees, the fence, etc., but another possibility is that they used odour trails laid down by themselves during previous foraging bouts, or that they were responding by smell to peanuts or peanut residues. We think this is unlikely for four reasons. First, when the pattern of baiting was changed on trial 8 (retraining trial) the badgers responded to the new pattern, not to the old one as would be expected if they were following odour trails or bait residues left over from the previous night. Second, the experimental patches were regularly visited by other badgers both before and after visits by the animals whose results are reported here, and different baiting patterns were used for different individuals. Thus the whole area must have become an impenetrable maze of superimposed odour trails. Third, although badgers do regularly mark the environment with secretion from a caudal gland, and although it has been suggested that the function of this marking is to tell an animal where it has recently been (e.g. Neal 1977), we only once saw a badger engaging in caudal marking during a visit to the test area.

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Finally, badgers do seem to have reasonable visual sensitivity at night a n d they react with suspicion towards a novel object (such as an observer) that appears in a n u n a c c u s t o m e d position within their visual range. It therefore seems certain t h a t they have a precise idea o f the location of potential l a n d m a r k s such as trees, shrubs, clumps o f grass, etc., within their h o m e territories. I n conclusion, our results suggest two mechanisms whereby badgers achieve efficient foraging behaviour: area restricted foraging u p o n e n c o u n t e r i n g a prey item, and m e m o r y of previous distributions o f prey based on the use o f distal landmarks.

ACKNOWLEDGMENT This research was s u p p o r t e d by a Royal Society grant to T.J.R.

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Krebs, J. R. 1978. Optimal foraging: decision rules for predators. In: Behavioural Ecology: An Evolutionary Approach (Ed. by J. R. Krebs & N. B. Davies), pp. 23 63. Oxford: Blackwell. Krebs, J. R. & McCleery, R. H. 1984. Optimization in behavioural ecology. In: Behavioural Ecology: An Evolutionary Approach. 2rid edn (Ed. by J. R. Krebs & N. B. Davies), pp. 91-121. Oxford: Blackwell. Kruuk, H. & Parish, T. 1981. Feeding specialization of the European badger Meles meles. J. Anim. Ecol., 50, 773-788. Kruuk, H. & Parish, T. 1982. Factors affecting population density, group size and territory size of the European badger Meles meles. J. Zool., Lond., 196, 31 39. Morris, R. G. M. 1981. Spatial localization does not require the presence of local cues. Learn. Motiv., 12, 239-260. Neal, E. 1977. Badgers. Poole, Dorset: Blandford Press. Pyke, G. H. 1981. Optimal foraging in nectar-feeding animals and coevolution with their plants. In: Foraging Behavior: Ecological, Ethological and Psychological Approaches (Ed. by A. C. Kamil & T. D. Sargent), pp. 19 38. New York: Garland STPM Press. Roper, T. J., Shepherdson, D. J. & Davies, J. M. In press. Scent marking with faeces and anal secretion in the European badger (Meles meles): seasonal and spatial characteristics of latrine use in relation to territoriality. Behaviour. Satchell, J. E. 1983. Earthworm Ecology. London: Chapman & Hall. Sherry, D. F. 1982. Food storage, memory and marsh tits. Anim. Behav., 30, 631 633. Smith, J. N. M. 1974. The food searching behaviour of two European thrushes. II. The adaptiveness of the search path. Behaviour, 49, 1-61. Thomas, G. 1974. The influence of encountering a food object on subsequent searching behaviour in Gasterosteus aculeatus. Anim. Behav., 22, 941-952. Tinbergen, N., Impekoven, M. & Franck, D. 1967. An experiment on spacing out as a defence against predation. Behaviour, 28, 307-321. Zach, R. & Falls, J. B. 1976. Foraging behaviour, learning and exploration by captive ovenbirds (Aves: Parulidae). Can. J. Zool., 54, 1880-1893.

(Received 24 April 1985; revised 24 October 1985; MS. number: 2691)