Predator odour per se does not frighten domestic horses
Introduction
Predation is a strong selective force leading to various adaptations in prey species. Many species have developed specific behaviours to facilitate recognition, avoidance and defence against predators. Such anti-predator behavioural systems are fundamental to survival, and natural selection has favoured mechanisms in prey to detect predators prior to their attack, increasing the probability of escaping or avoiding encounter (Kats and Dill, 1998, Apfelbach et al., 2005, Monclús et al., 2005). Anti-predator defence can involve responses to specific chemical cues that predators produce, and avoidance of predator odours, such as fur, urine, faeces, or anal gland secretions, has been observed in several mammalian species, particularly in rodents (for review see Apfelbach et al., 2005). It has also been shown that odour-induced unconditioned fear in rodents is associated with Hypothalmic-pituitary-adrenal (HPA) and amygdala activation (Dielenberg and McGregor, 2001, Li et al., 2004, Roseboom et al., 2007, Takahashi et al., 2007). Recent studies have suggested that skin and fur-derived predator odours may have a more profound and lasting effect on prey species than those derived from urine or faeces (Apfelbach et al., 2005). Studies on domestic herbivores, such as sheep and cattle, have demonstrated behavioural changes (Terlouw et al., 1998) and reduced feeding (Pfister et al., 1990, Arnould and Signoret, 1993, Arnould et al., 1993) in the presence of dog faeces. Highly distinctive smells, such as that of carnivore faeces, may however interfere with the experience of taste which may in turn cause reduced feeding, without the animal actually being frightened by the odour. Thus, both behavioural and physiological measures should be considered, because the body's immediate physiological reaction to perceived danger is characterised by activation of the sympathetic system (fight or flight response; Guyton and Hall, 1997, Korte, 2001). However, physiological measures have rarely been used in studies of predator recognition in herbivores because the majority of studies have been carried out in the field where such measures are difficult (Apfelbach et al., 2005, Monclús et al., 2005, Monclús et al., 2006). In this study we have recorded behavioural reactions in combination with recordings of heart rate, which have been validated as a reliable and non-invasive physiological measure in horses during exposure to a stressor (Visser et al., 2002, Christensen et al., 2005, Christensen et al., 2006, McCall et al., 2006).
Ungulates have co-evolved with their predators for millions of years in the wild, and like many other prey species they have evolved anti-predator responses both to actual encounters with predators and to generalised threatening stimuli, such as loud noises and sudden events (Frid and Dill, 2002). Equids typically live in open grasslands with a good view of the surrounding environment and they use vision as a major sensory avenue for detection of predators. Equids are also sensitive to auditory signals of danger, such as sounds of predators, and they have a good sense of hearing (Heffner and Heffner, 1983, MacDonald, 1995). In addition, equids may use olfaction as another modality through which predators can be detected and possibly identified. Chemical signals have been suggested to be involved in several equine processes such as individual identification, co-ordination and spacing of individuals both within and between social groups, mare-foal communication, navigation and orientation, sexual arousal and performance, as well as alarm signalling (Mills and Nankervis, 1999, Waring, 2003). Accordingly, there is a general belief among riders that horses are innately frightened by certain odours. However, we have currently no knowledge of whether horses do find certain odours aversive. A study by Christensen et al. (2005) showed that domestic horses reacted more to unknown visual and auditory stimuli compared to an unknown olfactory stimulus (eucalyptus oil). It is unknown, however, whether this lack in response applies to natural odours as well.
Here we present results from three experiments, in which we investigated how horses respond to (i) urine from wolves and lions, (ii) blood from conspecifics and fur-derived wolf odour, and (iii) a sudden auditory stimulus in either presence or absence of fur-derived wolf odour.
Section snippets
Animals
We used a total of 45 two-year-old Danish Warmblood horses from a large stud in the three experiments (Experiment 1: 33 stallions; Experiments 2 and 3: 12 mares). All horses were kept on pasture with the dam before weaning (approx. 6 months) and were subsequently kept in large groups of same age and sex; housed in straw-bedded group boxes during the winter and pastured during summer. The horses had received a minimum of handling at the stud, and had been handled only for other research
Experiment 1: predator urine
Horses that were exposed to urine from wolves and lions spent significantly more time sniffing compared to those exposed to horse urine (seconds, mean ± S.E.: Lion: 19.6 ± 4.4, Wolf: 16.5 ± 4.8, Horse: 1.2 ± 0.6; F2,30 = 6.83, P = 0.004). Also, we found a tendency towards an increased number of eating bouts in the wolf and lion group (freq., mean ± S.E.: Lion: 5.2 ± 0.4, Wolf: 4.8 ± 0.4, Horse: 3.9 ± 0.3; F2,30 = 2.94, P = 0.068). However, there was no significant effect on any other behavioural variables (e.g.
Discussion
Our results demonstrate that domestic horses show only minor behavioural reactions to the odour of predator urine in a known environment, and some investigative behaviour (e.g. increased sniffing and focussing on other stimuli), but no increase in heart rate, to fur-derived wolf odour and blood from a slaughtered conspecific. However, the introduction of additional cues of danger, i.e. a sudden auditory stimulus, caused horses in the presence of predator odour to show stronger flight reactions,
Acknowledgements
Thanks to Viegaard Horse Stud for allowing us to use their horses; to Director Richard Østerballe, Givskud Zoo, for collection of predator odours; to Dr. Jens Malmkvist, Dr. Birte Lindstrøm Nielsen, University of Aarhus, Prof. Jan Ladewig, University of Copenhagen, and Prof. Linda Keeling, Swedish University of Agricultural Sciences, for help and comments. This study was funded by a SLU strategic research fund for horses (Hippocampus) and by the Danish Research Council for Technology and
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