We tested the hypothesis that known individual badgers would demonstrate relative preferences for four bait types (three repellent-treated and one untreated). We established that wild mammals could develop CTA to a food-based repellent and then discriminate efficiently between treatments, thereby avoiding aversive baits without sampling. Once acquired, the aversion was maintained without additional reinforcement for the remaining 12–22 treatment nights (24–44 trial nights). This has implications for the protection of untreated foods from wild animals. Detailed behavioural analysis allowed us to observe the exact pattern of events taking place, and so deduce that the mechanism most likely involved was second-order conditioning. We believe that the results presented here already point to circumstances where such methods can be useful to wildlife managers.
We tested repellents together to assess their relative effects in a cafeteria-style experiment, adapting the methodologies of Andelt, Burnham & Manning (1991) and Andelt, Burnham & Baker (1994). This approach allowed comparison of individual badgers’ responses to the three repellents, while avoiding potentially confounding effects arising from prior experience, seasonal changes in natural food availability, behaviour or motivation to feed (Rogers 1974; Nolte & Barnett 2000). As a result, we are cautious in our conclusions regarding the likely effect of the compounds in isolation. Nevertheless, the effects of ziram were so clear here that it is difficult to believe that they would be less so in the absence of the other treatments. Furthermore, the badgers’ ability to discriminate precisely between the various treatments in our study is of practical predictive value, because free-ranging omnivores rarely spend a night consuming a single food (Macdonald & Barrett 1995). This suggests that the CTA, which badgers appeared to develop here, could allow them to avoid target food while continuing to eat alternative foods (Dimmick & Nicolaus 1990) and maintaining their territorial role (Nicolaus & Nellis 1987).
Ours was a conservative test of repellency, because the 68-night pre-trial phase probably created a significant expectation that foods at the site would be palatable. Also, repeated sampling of ‘safe’ untreated baits in the pre-trial may have endowed treated baits with some degree of learned safety, a phenomenon that has been shown to attenuate the development of CTA (Kalat & Rozin 1973). In addition, the majority of Wytham badgers do not survive beyond their fourth year (Macdonald & Newman 2002) and our sample was biased towards older animals (three of the four most regular visitors were between 5 and 13 years old), with extreme toothwear and in poor body condition. Such animals, if less able to forage naturally, may be more likely to become pests, so providing a good model for this research.
There was little between-individual variation in treatment responses. The consistency of bait patch rejection and other behaviour towards untreated baits, on pre-trial, treatment and control nights, indicated that there were no seasonal effects and that badgers had not formed general aversions to the site or to untreated baits. One possible exception might have been badger 70, which stopped attending after four treatment nights.
capsaicin and cinnamamide
Badgers appeared not to discriminate between capsaicin, cinnamamide and untreated baits on the first treatment night (Fig. 5), but thereafter formed a clear preference for untreated baits, followed by cinnamamide and capsaicin in no particular order, and then ziram. This preference was apparent in diverse behavioural measures (first-choice responses, bait patch rejection and order eaten), but would not have been detected by measuring bait consumption alone.
Badgers ate capsaicin, cinnamamide and untreated baits with equal eagerness on the first treatment night, which suggests that neither capsaicin nor cinnamamide, was immediately aversive, although capsaicin is considered to be innately repellent to mammals (Mason et al. 1991). Neither repellent proved promising as a feeding deterrent for badgers at the concentrations tested. Ultimately, we could not discriminate between the badgers’ treatment of capsaicin and cinnamamide, so while the reasons may have been different, the general measure of aversion to these two substances was similar.
Badgers preferred all other baits over those treated with ziram. On the first and second treatment nights, they finished ziram baits last, suggesting some innate avoidance of the taste (or irritancy) of ziram (Merck 1989). We used ziram incorporated with a ‘sticking agent’, a commercially available repellent formulation marketed as AAProtect™ (CAB International & the British Crop Protection Council 2001). AAProtect™ has an odour, acquired during manufacture, that is detectable to humans; this wanes as the formulate dries. If badgers were deterred at all by this odour, this was not sufficient to prevent them from approaching and eating ziram baits initially. Between T3 and T9 (fifth and seventeenth nights from first exposure), badgers left an increasing proportion of ziram baits uneaten. This decline in ziram consumption coincided with a sharp increase in the patch rejection behaviour associated with each repellent. Patch rejection peaked around the seventh treatment night (thirteenth from first exposure) before returning to previous levels (Fig. 4). Ziram bait consumption was practically zero over the last 20 treatment nights (40 trial nights). Individuals avoided ziram baits at a distance for the last 12–22 treatment nights (24–44 trial nights), and sampled them only very rarely. After eating all other baits, badgers often returned to walk around at the site, apparently ignoring the intact ziram baits (similar behaviour has been observed among racoons with CTA towards eggs; Semel & Nicolaus 1992). Our badgers stopped eating baits abruptly following full consumption, a feature characteristic of CTA (Dimmick & Nicolaus 1990). Under these conditions, it appears that ziram generated CTA in badgers.
Each of the regular visitors in this study demonstrated an individual pattern of sampling, and individuals stopped sampling ziram at different stages of the trial phase. This suggests that there was no significant social transmission of CTA. Although social communication about foods has not been studied in badgers, research on racoons and Norway rats Rattus norvegicus indicates that CTA is not socially transmitted to naive individuals (Semel & Nicolaus 1992; Galef 1997).
Taste is generally more likely to become associated with illness than other cues (Garcia & Hankins 1977), because taste and visceral information are processed in the same part of the brain (nucleus solitarius) whereas that relating to odour, and other non-taste cues, is not (Garcia, Clarke & Hankins 1973). When an undetectable agent causes CTA, the animal subconsciously associates the taste of the food with the illness produced, and subsequently avoids the taste of the food as a result (Garcia, Kimeldorf & Koelling 1955). Our badgers discriminated between baits according to treatment, indicating that they were able to detect ziram, and consequently developed an aversion to the taste of ziram (probably through post-ingestional effects), rather than to the taste of the baits themselves (Cowan, Reynolds & Gill 2000). Indeed, many naturally occurring toxins that produce CTA are highly flavoured (Nicolaus 1987) and may function in this manner.
When CTA develops, either to the taste of food or the taste of a detectable repellent, the target animal would have to bite or lick the food each time before being averted (Gustavson et al. 1974, 1976). This might necessitate the food becoming damaged (or killed) (Gustavson et al. 1976; Nicolaus & Nellis 1987). Avoidance without sampling is therefore key to protecting untreated foods; in fact, extinction of aversions is usually a result of sampling (Testa & Ternes 1977). Nicolaus and co-authors, have performed a number of studies testing CTAs as wildlife management tools for the protection of untreated foods from damage by free-ranging racoons, mongooses Herpestes auropunctatus and guilds of mammalian predators including American badgers Taxidea taxus. In these studies, animals avoided untreated foods at a distance, probably through second-order conditioning or potentiation (Nicolaus, Hoffman & Gustavson 1982; Nicolaus & Nellis 1987; Nicolaus et al. 1989c; Semel & Nicolaus 1992). Second-order conditioning is a two-stage process: first, the taste of food becomes aversive when paired with illness; secondly, non-taste cues become associated with the now aversive taste, and themselves inhibit approach or attack (Gustavson et al. 1974). Potentiation is a one-stage process whereby a weak cue for illness, for example odour or colour, can be facilitated to become a strong cue (Garcia & Rusiniak 1980; Westbrook, Clarke & Provost 1980).
Up to the night on which badgers stopped eating ziram baits, our behavioural analyses revealed an increase in patch rejection behaviour towards repellent-treated baits, and in particular ziram (Fig. 4). We conclude that, despite simultaneous presentation of four bait types, badgers developed CTA to the taste of ziram baits, and then second-order conditioning took place over this period of increased sampling/rejection. Badgers then avoided ziram baits, without further direct sampling, using odour as the aversive cue. The important question is whether they would have continued to avoid untreated baits that produced the same cues (Nicolaus et al. 1983). Such a phenomenon might be used to protect untreated foods that are destined for human consumption (e.g. crops, grain, eggs and fruit; Gustavson 1977; Nicolaus & Nellis 1987; Nicolaus 1987; Nicolaus et al. 1989a; Semel & Nicolaus 1992). However, the situation is not straightforward.
There are two ways in which CTA to an odour cue might theoretically be used to protect untreated foods from sampling: (i) a CTA agent, undetectable or detectable, could be used to create an aversion to the taste (of the food or the agent, respectively) and odour of the target food, such that conditioned animals subsequently avoided the odour of the food itself; or (ii) a bi-sensory aversive agent [combining a CTA agent (undetectable or detectable) with a novel, benign and effusive odour] could be used to create an aversion to the taste (of the food or the agent, respectively) and the odour cue provided, with the aim that target animals would subsequently avoid the odour cue. The odour might then be used to reduce feeding damage in sensitive areas.
It would seem preferable to use an undetectable CTA agent. The potential drawback of using an agent with a detectable taste, such as ziram, is that any olfactory barrier (whether natural food odour or added odour cue) may be breached, and the untreated food will taste different from the ziram-treated food that caused the original illness. However, no CTA agents that are undetectable and sufficiently safe have yet been registered for use. Even oral oestrogen, a uniquely successful undetectable CTA agent, may act as an abortifacient or teratogenic (Reynolds 1999). It is extremely unlikely ever to be registered as a repellent (or for any environmental use) in the UK. Nevertheless, despite the potential drawback of using a detectable aversive agent, our results demonstrated that badgers did not breach the odour barrier to sample ziram baits for the last 12–22 treatment nights (24–44 trial nights). This may well have been sustained if the experiment had continued. We conclude that: (i) badgers can learn to avoid foods on the basis of odour without sampling; and (ii) while the search continues for safe, undetectable CTA agents, we should further investigate the use of ziram (Baker et al., in press a, in press b ). The next step is to develop appropriate management strategies through field trials.
CTA particularly lends itself to the protection of foods that are vulnerable for fixed, predictable periods, for example crops susceptible to badger damage for a few weeks before harvest. Protection would therefore be required for this limited period only (Wilson 1993; Moore et al. 1999). We propose that a bi-sensory agent combining ziram with a novel, effusive odour cue, for example clove oil, might be used for this purpose (Baker et al. in press b). An irritating, or unpleasant-smelling, odour would prove undesirable and impractical (for humans and non-target species) for use in real-life wildlife management situations, whereas a novel, effusive odour should be readily associable and unlikely to have previously acquired connotations. For example, in order to protect a maize crop from badger damage, maize cobs treated with the bi-sensory agent could be dispersed on the ground around the growing crop and at the local badger setts. Treatment should take place prior to the predicted time of damage (Avery & Decker 1994), to prevent cobs acquiring learned safety through badgers sampling the ‘safe’ untreated ripening crop before conditioning begins and to allow sufficient time for the aversion to develop, i.e. for the learning curve to take place. The clove odour (alone) and sacrificial cobs (treated with the bi-sensory repellent) would be replenished throughout the sensitive period to reinforce the aversion.