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Influence of predator odour on the feeding behaviour of the root vole (Microtus oeconomus Pallas, 1776) Zbigniew Borowski

Abstract: An experiment carried out under laboratory conditions addressed the influence exerted by the odour of a stoat, Mustela erminea Linnaeus, 1758, on the feeding behaviour of a root vole, Microtus oeconomus Pallas, 1776. Specifically, the impact of the odour on the chewing of rowan (Sorbus aucuparia) shoots and consumption of food pellets by voles that were not sexually active was observed over a 14-day period. The floors of cages with individuals from the experimental group were sprinkled daily with a distilled-water rinse from a glass clamber in which a stoat had been confined, while cages holding control individuals were sprinkled with distilled water only. The uptake of food was monitored daily by checking the degree to which shoots had been chewed, as well as the amount of food pellets consumed. Stoat odour caused a significant reduction in chewing of the shoots but did not affect the amount of food pellets eaten. There was no significant influence of the scent on body mass, which suggests that the assimilation of food was probably the same for voles in the experimental and control groups. Long-term exposure to stoat scent was not associated with changes in food consumption over time, which suggests that the voles had not become habituated to the presence of the odour over the 2-week period. It would therefore seem that the stoat scent affected the specific feeding behaviour of the voles rather than their overall consumption level. Résumé : Une expérience dans des conditions de laboratoire a permis d’étudier l’influence de l’odeur de l’Hermine (Mustela erminea Linnaeus, 1758) d’été, sur le comportement alimentaire du Campagnol nordique, Microtus oeconomus Pallas, 1776. Spécifiquement, l’impact de l’odeur sur le mâchement des racines du sorbier Sorbus aucuparia et sur la consommation de boulettes de nourriture par des campagnols inactifs sexuellement a été observé durant 14 jours. Le plancher des cages des animaux expérimentaux a été arrosé chaque jour avec de l’eau distillée de rinçage d’une cage de verre où une hermine avait été confinée, alors que le plancher des animaux témoins n’a été arrosé qu’avec de l’eau distillée. La consommation de nourriture était évaluée chaque jour par estimation de la quantité de racines mâchées et de la quantité de boulettes mangées. L’odeur d’hermine a entraîné une importante réduction du mâchement de racines, mais elle n’a pas affecté la consommation des boulettes de nourriture. L’odeur n’a pas eu d’influence significative sur la masse des campagnols, indiquant probablement que l’assimilation de nourriture était équivalente chez les deux groupes d’animaux. Une exposition prolongée à l’odeur d’hermine d’été n’a pas modifié la consommation de nourriture, ce qui indique que les campagnols n’ont pas développé d’habituation à la présence de l’odeur pendant les 2 semaines d’exposition. Il semble donc que l’odeur d’hermine d’été affecte le comportement alimentaire spécifique des campagnols, plutôt que leur consommation globale de nourriture. [Traduit par la Rédaction]

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The influence of the odour of a predator on the behaviour of members of the vole family has been recognized in ecology for more than 20 years (Stoddart 1976). In the light of results obtained, and considering the theory of evolution, it would seem that the greatest influence on potential prey will be exerted by the scent of a predator with which it has coevolved. Prey and predator species may have participated in their own kind of “arms race” (Dawkins and Krebs 1979), as a result of which the prey species “learned” to read information contained in the odour of predators and to respond appropriately. In spite of the very similar chemical composition of the odours of different mustelids (Brinck et al. 1983), Received September 9, 1997. Accepted March 19, 1998. Z. Borowski. Forest Research Institute, Section of Wildlife Management, Bitwy Warszawskiej 1920r. 3, 00–973, Warsaw, Poland (e-mail: [email protected]). Can. J. Zool. 76: 1791–1794 (1998)

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voles, for example, are able to recognize the species of predator and react accordingly (in relation to the hunting strategy of that species) (Jedrzejewski et al. 1993). Attesting to the persistence of the reaction of voles to the scents of mustelid predators is the fact that, even after 5000 years of isolation from the latter, voles resident on the Orkney Islands still display a strong negative reaction to the odour of a stoat (Mustela erminea Linnaeus, 1758) (Gorman 1984). This reaction may be explained in two ways. First, information concerning voles’ reactions to the scent of a predator is passed on genetically (Ylönen 1994). This hypothesis, however, may be questioned; research done with house mice (Mus musculus Linnaeus, 1758) conducted on an island without any predatory mammals showed that reaction to predator odour (cat, Felis catus, and red fox, Vulpes vulpes) may disappear after a certain number of generations (Dickman 1992), and therefore is not passed on genetically. The strong negative reactions of voles to stoat odour on the Orkney Islands may also be explained in a different way: © 1998 NRC Canada


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another predatory mammal may have been present on the islands. According to Dickman and Doncaster (1984), similar chemicals that elicit avoidance in rodents may occur in the faeces and urine of many eutherian carnivores. The scents of mustelids may have an impact upon both the behaviour and the physiology of voles. Observations on the influence of a weasel’s scent on bank voles (Clethrionomys glareolus Schreber, 1780) reveal responses involving reabsorption of foetuses, blocking of the entry of females into oestrus, reduction in locomotory activity (so-called “freezing”), and changes in sexual behaviour, such as aggressiveness of females towards males and active avoidance of sexual contact (Ylönen et al. 1992; Jedrzejewski et al. 1993; Ronkainen and Ylönen 1994). In contrast, in the field vole (Microtus agrestis Linnaeus, 1761), aggression of males towards females has been observed, perhaps a result of disruption of the hormonal balance in the latter (Koskela and Ylönen 1995). Field research has shown that under natural conditions voles avoid food tainted with the scent of stoats or weasels (Gorman 1984; Z. Borowski, in preparation) and reduce the degree to which they chew fruit trees protected with a synthesized form of the scent from the anal glands of the stoat (Sullivan et al. 1988a). The results of these experiments appear to confirm that the scent of mustelids has a strong impact on the feeding behaviour of voles. In spite of its great ecological significance, there is little evidence of an impact on the consumption and collection of food under either laboratory or field conditions (in spite of the influence exerted on the physiology and behaviour of voles by the scent emitted by mustelids). The aim of the work described here was therefore to answer the question as to whether the odour of a stoat would influence consumption by root voles of the shoots of rowan (Sorbus aucuparia), a species they chew willingly, and their intake of other food.

shown that of five tree species investigated (beech (Fagus silvatica), maple (Acer negundo), rowan, lime (Tilia cordata), and oak (Quercus robur)) in Poland, rowan is the species most willingly eaten by both the root vole and the field vole (Z. Borowski, in preparation). Shoots and pellets were made available to the animals for exactly 24 h (between 11.00 and 11.00), after which the amount of food pellets eaten was determined from the difference in the numbers of pellets before and after exposure to the voles. To determine the amount of food pellets eaten, the cotton wool and cardboard were examined carefully. The procedure was the same for both the experimental and the control group, to ensure that the influence of searching on food intake was the same. The degree of damage to the shoots was assigned to one of four classes: 0, no traces of feeding; 1, up to 25% of the total surface area of the shoots chewed; 2, 26–50% of the total surface area of the shoots chewed; 3, more than 50% of the total surface area of the shoots chewed. The animals ate not only the bark but also the phloem and wood of the shoots presented. Just before the experiment, voles maintained in the laboratory were divided into an experimental group and a control group. Care was taken that the sex ratio and body masses of individuals in the two groups were identical. For the experimental group the odour of a stoat was applied to the bedding and for the control group it was not. The floors of cages holding the individuals from the experimental group were sprinkled once a day, prior to the provision of shoots and food pellets (the food itself was not treated with predator odour), with a rinse of predator odour in distilled water. This rinse was obtained by using 150 mL of distilled water to wash a 1.5-L glass container that had held a stoat for 1 h. The stoat was an adult female that had been taken from the wild population in Biebrza National Park in autumn 1996 and kept in the laboratory up to the time of the experiment. Ten millilitres of solution per cage were applied. The rinse was prepared daily just before the consumption of shoots and pellets was checked. The floors of the cages holding the control individuals were sprinkled with distilled water only. Voles in the control and experimental groups were kept in separate rooms between which there was no exchange of air. The experiment continued for 14 days, each vole being weighed before and after. All individuals survived the 2-week period.

Laboratory experiments carried out in February 1997 involved 16 root voles, Microtus oeconomus, 8 males and 8 females, that were not sexually active. The animals were taken from the wild population in Biebrza National Park, northeastern Poland, in November 1996, and were maintained in cages (3 per cage) in the laboratory up to the time of the experiment (Gebczynska and Buchalczyk 1969). During this time, conditions were the same as during the experiment, i.e., a temperature of 16°C and natural light (8.5 h light and 11.5 h darkness). They were given standard food: rabbit pellets from the Institute of Parasitology, Lomna-Las, 05–152 Czosnow (composition: Premix FK, phosphatized salt, chalk (calcium carbonate), wheat germ, dried grass, fish meal, soya meal, barley bran, and oats), water ad libitum, as well as carrot and apple. During the course of the experiment, voles were kept singly in plastic and metal cages with dimensions 30 × 30 × 40 cm, and cardboard and cotton wool were supplied as material for nest-building. To study the level of consumption of both the rowan shoots and the rabbit pellets, use was made of the so-called “cafeteria test,” which is widely used in such experiments (Partridge 1981; Hansson 1993). Each cage was supplied with a standard amount (50) of food pellets daily in a glass dish, water ad libitum, and two fresh, growing shoots of rowan, 20 cm long and 0.5 cm in diameter (placed in the cage in a vertical position). Rowan shoots were chosen for this experiment because previous laboratory research had

To check for differences in body mass that might have affected the consumption level, body masses of male and female voles were compared both within and between the experimental and control groups. No differences were revealed between the sexes in either the control (Mann– Whitney U test, p = 0.2; Table 1) or the experiment group (Mann–Whitney U test, p = 0.4857; Table 1) or between the body masses of all individuals selected for inclusion in these two groups (Mann–Whitney U test, p = 0.9591). To check if there were differences between the sexes in the degree to which shoots were chewed and pellets consumed, data were compared between the sexes in both the control and experimental groups. No such differences were found in either case (t test, p > 0.05; Table 1). For this reason, males and females were treated as a single group. The control group and the experimental group were compared to determine whether the stoat odour had influenced the consumption of rowan shoots. It was found that the shoots available to the voles exposed to stoat odour were chewed to a significantly lesser degree than those given to control individuals (t test, t = 4.69, p = 0.00008). In contrast, the control and experimental groups did not differ signifi© 1998 NRC Canada



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Table 1. Average daily consumption of rowan shoots and food pellets by root voles, and changes in their body mass after exposure to predator and control odours. Predator odour

Control

Shootsa

No. of pellets

Body mass (g)

Shootsa

No. of pellets

Body mass (g)

Males (n = 4) Females (n = 4)

1.88±0.93 1.53±0.73 t test, t = 1.62, p = 0.1101

20.1±9.91 18.43±11.61 t test, t = 0.65, p = 0.5208

2.35±0.9 2.31±0.8 t test, t = 0.16, p = 0.8724

22.35±7.62 19.72±7.82 t test, t = 1.45, p = 0.1524

Males and females (n = 8)

1.7±0.9

18.74±10.3

31.2±1.7 29.2±1.7 Mann–Whitney U test, U = 0.2, p = 0.2 30.2±1.9

30.1±3.0 31.7±2.8 Mann–Whitney U test, U = 5.0, p = 0.4857 28.1±3.4

2.4±0.8

20.82±7.81

a

On a scale of 0–3.

cantly in regard to the number of food pellets consumed (t test, t = 1.35, p = 0.1783). In turn, the data on body mass were analyzed with a view to determining whether predator odour had affected the assimilation of the food consumed. Again the groups were not found to differ significantly, this time in relation to differences in body mass before and after the experiment (Wilcoxon’s test for pairs, experimental group: W = 11.0, p = 0.1875; control group: W = 10.0, p = 0.437). Finally, a check was made of whether the uptake of food by voles had changed as the experiment progressed. To do this, the mean amount of pellets consumed and the mean extent to which shoots were chewed were compared between consecutive days for the experimental group (ANOVA, F = 0.728, p = 0.6720) and the control group (ANOVA, F = 0.212, p = 0.6508). No significant differences in food intake were noted, confirming similar levels of consumption throughout the experiment.

The chewing of shoots by individuals in the experimental group was found to be reduced under the influence of stoat odour, while the uptake of food pellets did not differ from that by the control group. This may attest to an impact of the odour on specific patterns of feeding behaviour, rather than on overall consumption, in this species of vole. All the more so since voles are not able to interrupt their food intake for longer periods on account of their high metabolic rate (Gebczynska 1970). The behaviour observed among the voles may be explained in two ways. On the one hand, it would seem that voles wishing to eat shoots must leave the nest, a behaviour associated with the threat of predator attack. Furthermore, vertically orientated shoots are more difficult to eat than a portion of food, suggesting that a vole engaged in eating the former would be more involved in the act of feeding. Thus, while eating shoots a vole would have a reduced opportunity to detect stimuli from the environment and react rapidly to them. The result would again be an increased risk of predation. Similar behaviour to that noted in voles, again entailing maximization of feeding efficiency and minimization of the duration of exposure to predators, has been recorded in grey squirrels (Lima et al. 1985). On the other hand, the animals studied may have treated the shoots as a supplementary source of food and minerals (Hansson 1990), the intake of which could be reduced with-

out a consequent decrease in body mass, when the risk of predation was high. The apparent lack of difference in body mass between the experimental and control animals may also attest to the fact that the odour of a stoat does not affect the assimilation of food. The fact that the amount of food consumed did not change over consecutive days of the experiment shows that the voles did not become habituated to the odour of the predator over 14 days. The animals maintained similarly low indices for the chewing of shoots between the first and last days of the experiment. Those seeking to apply a method that entails the use of mustelid odours for protecting tree seedlings and saplings from rodents should recall that all attempts to use such scents in natural conditions may meet with serious problems (Sullivan et al. 1988b; Borowski 1994). The reason is that voles mainly damage trees in the winter or early spring, when alternative, more nutrient-rich food like herbaceous vegetation is lacking (Buacyanayandi et al. 1992). For this reason, it is likely that, given the lack of alternative food, such as pellets under experimental conditions, tree seedlings and saplings will continue to be chewed during the aforementioned periods in spite of attempts to protect them with predator scents. It would seem that future work should focus on observing (perhaps by video-recording) the changes in feeding behaviour induced by the presence of a predator or its scent, as well as on experiments in which no additional food pellets are provided. Field research employing predator odours to protect trees from voles should also be done with a view to obtaining unambiguous answers as to the strength and directions of the impact of the scent of a predator on the consumption of food.

I am grateful to Prof. R. Andrzejewski, Prof. E. Szukiel, Prof. J. Gliwicz, Dr. J. Borkowski, and M.Sc. P. Nasiadka for their constructive comments on earlier drafts of this paper. The study was supported by grant No. BLP-702 awarded by the General Directorate of State Forests.

Borowski, Z. 1994. Use of predator odours to reduce feeding damage by rodents (Rodentia)—review. [In Polish with English summary.] Sylwan, 11: 113–121. © 1998 NRC Canada



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