Status concerning the welfare of farm foxes
University of Copenhagen, Zoological Institute, Tagensvej 16, DK-2200 Copenhagen N, Denmark
Rules and legislation on the housing of farm animals are often the result of a media-created debate between consumers, politicians and various "experts" (e.g. researchers, veterinarians, animal protection societies). At the moment the consumers are more conscious of the housing conditions of farm animals, and gradually they have also become willing to pay for goods which have been produced in a more ethically acceptable environment. It is therefore important that objective scientific results concerning the conditions of farm animals are available, the objectivity of which can guide the industry, politicians, and consumers in existing and future debates. Behaviourall research can contribute with knowledge about the normal behaviour of farm animals, which is one of the basic preconditions of being able to assess welfare, and it can show possible welfare problems and the farm animals' state of welfare and suggest solutions to welfare improvements.
Veterinary Services concerning Breeding of Game and Foxes (1997). Welfare-wise the demand for a resting platform for allfarm foxes is the most significant change compared with previous regulations. Finnish (a.o. Harri et al. 1991) and Danish (a.o. Pedersen & Jeppesen, 1993) studies have stressed that foxes use a resting platform to observe the surroundings both in quiet and disturbed situations, and having this possibility is important to the individual fox. Apart from this, the cage environment has been relatively unchanged for the past three decades, and there is no demand for any changes in the existing regulation. The Council of Europe has also in its recommendations concerning fox husbandry used recent years' Behavioural research. Among other things it recommends that breeding vixens have access to a whole-year shelter. Regarding the cage evironment, the Ministry of Agriculture has financed a 5-year project where alternative cage systems are tested for both blue and silver foxes. Considerable differences between the alternative systems and the traditional system are cage size and improvements such as resting platforms, whole-year shelter, solid bottom, and sand tray. The results are expected to reveal whether the considerable changes of the existing cage environment in fact lead to a significantly improved welfare of the farm foxes.
This paper summarises some of the most recent results of the research in the behaviour of farm foxes and lists the areas which will be focused on in the nearest future.
Behavioural research often focuses on breeding vixens when the effect of improving the cage environment is tested, while most of the studies of the production animals have concentrated on the man-animal relationship where attempts have been made to make the animals more trusting towards people. In a 3-year project, it has been shown that silver foxes fear of people is reduced by regular human contact during the early growth phase just before and after weaning. Besides reduction of fear, a reduced stress sensitivity and, later on, improved breeding results were seen (Pedersen, 1993). But what is the value of the man-animal relationship and the cage environment, respectively, for the welfare of the individual animal? Is one parameter more important to welfare than another? As far as blue foxes are concerned a thesis project performed at the University of Copenhagen tried to provide the answer to that (Bertelsen, 1996). A group of blue fox cubs were treated tenderly 5 minutes daily from 7 to 10 weeks of age. The other group was a control group which was only subjected to normal routines. All the cubs were tested for behaviour at the age of 10 weeks and thereupon distributed to cages with or without a whole-year shelter (cage environment). 'Me different behaviour tests showed that the handled cubs were less fearful towards people and less fearful generally compared with the control group. At the same time, cubs without a whole-year shelter were less fearful towards people and unknown objects compared with cubs with a whole-year shelter. At the age of 22 weeks, the cubs were subjected to a test in an unknown environment, a so-called "open field" test. Again it was shown that handled animals were more calm and curious during catching in their cages and in the open field test compared with the control group. No significant effect of cage environment was found on behaviour in the open field test, but a tendency opposite to that of the behaviour tests: namely that cubs with whole-year shelters were less fearful than cubs without whole-year shelters. Blood samples taken before the open field test were supposed to indicate the basic stress hormone level, and blood samples taken after the open field test should indicate the effect of acute stress on the cubs' stress hormone level. But results showed no effect of handling or cage environment on the stress hormone level. In the following breeding period, handled foxes showed a tendency to get more cubs, and more cubs survived the first 4 weeks compared with the control group.
The conclusion was that early handling of blue fox cubs significantly reduces their general fear as well as their fear towards people and thus increases their welfare. Physiological parameters could not confirm this relationship, but only that fearful foxes generally had a higher basic level of stress hormone
in their blood. Whether a whole-year shelter could improve the welfare of blue foxes during the growth period could not be proven due to the opposing results. The results indicated, however, that human contact at an early age had a greater influence on the welfare of blue foxes than cage environment (access to a whole-year shelter during the growth period).
Cage environment during the growth period
As far as we know, tests describing how different rearing conditions affect the blue fox cubs with regard to growth, behaviour, welfare and later reproduction have never been performed. Perhaps there exists an optimal procedure which: 1) secures the blue foxes optimal conditions during the growth period, 2) secures the breeder larger furs at pelting, or if the foxes are going to be used for breeding, 3) secures the breeder optimal reproduction results. Two different rearing conditions were tested with regard to behaviour, welfare and weight development in the growth period as well as weight and reproduction success in the following breeding period. The rearing conditions tested were rearing 'in pairs or solitarily from weaning and separation at the age of 7 weeks. Other parameters such as e.g. age at weaning and weaning in litters a couple of weeks before separation will be tested at a later stage.
The blue foxes were weighed several times during the growth and breeding period to describe growth and weight loss. Furthermore, behaviour was evaluated in two different tests where the trust of the foxes towards people and their general level of fear were registered. Reproductive success was measured by number of born and weaned cubs of mated and pregnant vixens as well as loss of cubs from birth until weaning. The two groups of blue foxes did not diverge significantly in any of the behaviour tests as approx. half of both groups were curious towards people and accepted titbits out of peoples' hands. And the curiosity towards an unknown object was equally high in both groups. Growth until pelting as well as weight loss until mating were higher in the group reared solitarily. In the same group (solitary rearing) a higher percentage of the vixens were either not mated or were barren compared with the group reared in pairs (23% to 6%). Effect of rearing conditions on number of cubs at birth and weaning could not be proven.
Based on these results it could be concluded that it is advantageous to rear blue foxes solitarily in order to obtain bigger animals at pelting, but in the long run it is advantageous to keep blue foxes in pairs from weaning as more vixens in this group reproduce. Based on the behaviour tests and the number of cubs, it could not be concluded that the welfare was threatened in either group, but all things considered the prevalence of non-reproducing vixens indicates a welfare problem. The reasons for the lack of reproduction should, however, be ascertained. In this case, the reason is probably the lack of sexual imprinting on own species in the growth period and is not necessarily stress-related. Further studies of behaviour and physiology would affirm or confirm whether solitary rearing affects the welfare of blue foxes in the short and long term.
For a period of 30 years, Russian researchers have selected for trust in farm foxes and have now obtained a population which is very trusting towards people and does not need demanding handling during the growth period. Precisely the lack of trust in farm foxes has been considered a significant welfare problem.. Therefore an initiative to a common Nordic project was taken in 1994, the objective of which was 1) to have more trusting foxes on private farms in Denmark, Finland, Norway and Sweden and 2) to examine the scientific and productional aspects of selection on behaviour. This project has been very well received by the participating breeders in Denmark (4 silver fox farms and 4 blue fox farms), and the first results have shown that trusting vixens of the selection group had more cubs than the other vixens on the farms (Pedersen, 1995). At the same time it became evident that more cubs born by trusting mothers are trusting at the age of 6 months compared with the cubs of the control group. Whether this trust is genetic or environmental cannot be determined for the time being. The most important thing, however, is that trust can be tested, trusting farm foxes exist, the trusting foxes have more cubs, and the trusting foxes have trusting cubs.
There is a theory in modem fox research that infanticide (cub killing) is based on a natural ability in individuals of the dog family (wolves, jackals, foxes etc.) to act as "helpers". "Helpers" abstain from reproduction but participate in the rearing of the litter
of the dominant vixen. It has also been seen in the wild fox that a vixen eats her own cubs whereupon she helps the dominant vixen to rear her cubs (MacDonald, 1979; 1980). Therefore, infanticide could be a natural occurrence of social behaviour and not necessarily an abnormal stress-related behaviour. This behaviour appears abnormal and extremely undesirable when otherwise healthy cubs have to be killed because of the higher social status of a neighbouring vixen, and because the vixen performing infanticide cannot perform the help function which caused the infanticidal act under normal farm conditions.
Bakken (1993) has examined the occurrence of cub killings in farm bred silver foxes of either very high or very low social status. This kind of basic research can be used to affirm or confirm the theory that cub killings in farm foxes are caused by social mechanisms. And the Norwegian results indicate that social status among neighbouring vixens affects reproduction success so that low-ranking vixens have a bad reproduction when the neighbouring vixen is high-ranking. On private farms, however, there is a far greater variation of social status among the vixens, e.g. because of differences in age, high replacement rate and frequent removal of the vixens. It would, therefore, be interesting to examine the stability of social status in an ordinary farm fox population and study the effect of social status on different welfare parameters. Three Danish projects aimed to examine this complex of problems, out of which two have been finished and the third will be terminated in 1998.
Project 1: 'Me social status, behaviour and physiology were examined in silver fox vixens kept in pairs in a thesis project at the University of Copenhagen (Bank, 1996). Furthermore, the effect was examined of an acute (single) stressor and repeated stressors, respectively, on different behavioural and physiological parameters in the dominant and subordinate (inferior) vixens. Sixty unrelated silver fox vixens were paired off randomly. These vixens were tested for social statusi 8 times with a test procedure developed by Morten Bakken (Feed Competition Capacity Test, FCC-test, Bakken, 1993). In this test, the vixens compete for access to attractive feed after 24 hours without feed. The test was also performed with a ball as the competitive object (OCC-test). The vixen who was in possession of the feed for at least twice as long as the other vixen, was classified as dominant and the partner as subordinate. All the vixens were exposed to an acute stressor (open field test) with blood sampling before and after the test. Half of the vixens (30) were exposed to repeated stressors, i.e. the open field test was repeated 8 times for each animal, without blood sampling, however. Finally, all vixens were exposed to an ACTH-stressor. ACTH is injected to make the adrenal glands produce stress hormones. The reaction of the adrenal glands to the ACTH-stressor provides information on the general stress level of the animal.
Results showed that the FCC and OCC-tests could not in all cases determine the vixens' social status, and when it could be determined, it was not stable in the course of a 6-month period. Furthermore, there was not agreement between the FCC and the OCC-test in the determination of social status as only 50% of the pairs had the same score in the two tests. There was no significant effect of social status on the measured behavioural and physiological parameters. Subordinate vixens, however, tended to be more passive in the tests than dominant vixens. Repeated stress affected the vixens but did not result in long-term stressed vixens, which was expected. Repeatedly stressed vixens showed signs of a passive tolerance to handling and the results of the physiological measurements indicated that they were less stressed on a daily basis compared with the acutely stressed vixens.
These results stressed that social status in randomly chosen fox vixens cannot be determined fairly on the basis of a single or a few tests as the dominance relationship among the vixens can change in a short time, and as there were no standardised results when the competition object was food and object The non-significant results in behaviour tests and in physiological objectives seem to be due to the unstable dominance relationship. On the other hand, the results show that the daily farm routines were of greater importance to the welfare of the foxes than their mutual social status.
Project 2: In her thesis, Lise Overgaard continued to work with the above-mentioned dominance-tested vixens in the heat and breeding period (Overgaard, 1997). Each pair was placed in two adjacent cages, each with access to a shelter. The shelters were placed with the largest possible distance from each other, and shields were put up to hide other neighbours, so that only the two who were used to being together could see each other. During the heat measurement, the catching reactions of the vixens was observed. Furthermore, 3 behaviour tests and daily scanning observations to establish the use of shelter from birth and four weeks ahead were carried out during pregnancy. Cubs were counted often to register mortality, sex was determined and they were weighed at the age of 4 and 8 weeks.
The results indicated that the repeated stress to which half of the vixens had been exposed before the breeding period had caused a tolerance to farm routines for some vixens but also symptoms of a chronic state of stress in other vixens. Vixens who had been exposed to repeated stress bore and weaned fewer cubs compared with vixens exposed to only a single stressor (not significant), but the overall picture of the results did not show any difference in welfare between acutely stressed and repeatedly stressed vixens. Dominant vixens were generally calm (curious) in the various behaviour tests before and during pregnancy, while subordinate vixens often showed signs of fear or were passive. Dominance status did not affect reproductive success clearly, but on average dominant vixens bore and weaned a few more cubs than subordinate vixens (not significant). This result suggests that the dominant vixens experienced a slightly better welfare than the subordinate vixens.
The conclusion of the project was that there was only a small effect of dominance status and various earlier stress on the later reproduction success of a vixen. It seems possible, however, to improve the welfare of some vixens by accustoming them to farm routines (repeated stress), and to improve reproduction of foxes if status and behaviour are considered in the selection process.
Project 3: The third project is being carried out for the Faculty of Science, University of Copenhagen in 1997 and 1998. The objective of this project is to illustrate the occurrence of helpers and their social role in the wild population of foxes in Denmark, and to obtain a detailed knowledge of the social behaviour and reproduction of vixens held in groups through experimental tests. This article solely describes the preliminary results of the experimental part of the project.
Eleven groups were placed in separate aviaries of 28.8 m2. The aviary was fumished with various resting platforms and several whole-year shelters where the foxes could spend their time. The first year the group consisted of three unrelated adults (1 male and 2 vixens), where the vixens were of different colour types for the sake of identification. The foxes were put together in January and observations of behaviour and interactions of the match were registered. Weekly tests and scannings of the use of aviary and equipment as well as of social behaviour have been performed concurrently with registration of births and possible infanticidal behaviour. To sum it up, the litters and the role of the adults in relation to the cubs were registered and followed until the cubs were 16 weeks old.
Only in two of the groups did both vixens have cubs that all survived. In both cases, the cubs were born with a few days' interval in different shelters, and after three days the vixens brought the cubs together in one shelter. Hereafter only one vixen suckled the cubs while the other vixen stopped producing milk. .Later this vixen participated in the care of the cubs on equal terms with the other vixen. In these two groups, the dominant vixen adopted the litter of the subordinate vixen in one of the cases, and in the other case vice versa: the subordinate adopted the litter of the dominant vixen. Another group had two litters, but the subordinate vixen who had cubs first ate or killed her cubs 3 days before the dominant vixen whelped. All the cubs of the dominant vixen survived, and the subordinate vixen participated actively in the care of the cubs. In two groups only the dominant vixen had cubs, and the subordinate vixen was treated very aggressively and was kept away from the cubs and the shelter. In four of the groups, only the subordinate vixen had cubs and all the cubs were either killed or eaten, and in the last two groups there were no cubs. In all cases, the male played a minor role in relation to the cubs, but he was tolerant towards them and often brought them food when they left the shelter.
So it was a somewhat confusing picture emerging from the groups. It could not be established whether it was the lack of heat period or mating, sterile vixens, or absorbed foetuses causing the lack of litters in several of the vixens, but the high occurrence of infanticide and the fact that most often it was the subordinate vixen performing it, support Bakken's (1993) results: there is a social connection between status and infanticide in farmed silver foxes, also when they are housed together and physical contact is possible. It should be stressed, however, that it was possible for both vixens in a group to have cubs who all survived. If the reason could be established why exactly those vixens could live together and reproduce in harmony, we might have discovered a toot which could help to reduce socially conditioned infanticide on fox farms.
Recent years' behavioural research stresses the importance of a positive man-animal relationship both with blue foxes and silver foxes. Handling routines are, however, so time consuming that it could hardly be implemented on large fox farms. But if behaviour is taken into consideration in the selection of vixens, and the farmer keeps a trusting instead of a fearful vixen, the level of fear in the foxes will be reduced in the long run.
Infanticidal behaviour seems first of all to be caused by social mechanisms based on the natural ability of the species that individuals may act as helpers. This ability can probably not be eliminated by selection, but in some vixens it does not express itself even though they are housed together. Being unstable in the long run, it is difficult to work with social status on farm level. Curious and calm vixens probably have a higher status compared with fearful vixens, a fact that can be used in the selection process. But the effort of research should now be concentrated on the reason why vixens are able to reproduce successfully when housed together.
Bakken, M. 1994. Infanticidal Behaviour and Reproductive Performance in Relation to Competition Capacity among farmed Silver Fox Vixens, Vulpes Vulpes. Dr. Scient afliandling, Zoologisk Institut, Det Matematisk-Naturvidenskabelige Fakultet, AVH Universitetet i Trondheim.
Bank, L. 1996, Stressrespons ved Akut og Gentaget Belastning Relateret til Social Status hos Solvrmvetmver. Speciale i Etologi, Zoologisk Institut~ Kobenhavns Universitet.
Bertelsen, N. 1996. Effekt af Tidlig Stimulering og Adgang til HelArskasse hos BlAmve (Alopex Lagopus). Speciale i Etologi, Zoologisk Institut, Kobenhavns Universitet.
Harri, M., Mononen, J., Korhonen, H. and Haapanen, K. 1991. A Study of the Use of Resting Platforms by Farmbred Blue Foxes. Appl. Anirn. Behav. Sci., 30:125-139.
Macdonald, D.W. 1979. Helpers in a Fox Society. Nature, 282:69-71.
Scientifur, Vol. 22, No. 2, 1998