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Psychological stress in wild animals

Stress is commonly defined as a physiological response to a stimulus (a stressor) perceived by an individual as threatening or harmful, usually “produced by excessive environmental or psychological pressures”.1 It causes the buildup of adrenalin and cortisol hormones which leads to an increase in the heart rate and blood pressure and to a suppression of the immune system, among other ill effects to the health. It can sometimes be lethal, because it can lead to arrhythmias or heart attack.

While the effects of stress in domestic animals have been well documented,2 the severity and number of stressors that afflict wild animals have been underestimated by scientific research, except for the effects of captivity on wild animals. In light of this, some may think that stress plays little or no role in the wild, though this is far from being the case. Wild animals have to face very adverse circumstances on a daily basis that are usually stressful for them: physical trauma, disease, food shortages, conflicts with others of their species or herd, etc. However, few aspects of an environment seem to lead to more stress than predation.

Predator-induced stress seems to arise in two major scenarios. First, the scenario involving the predatory activity itself, in which animals face the awfulexperience of fleeing and/or fighting that usually precedes their death. The confrontation with the predator may be so intense that the animal preyed upon dies of stress.3 Wild rats have died of heart attacks after being forced to listen to a tape recording of a cat-rat fight.4

Second, stress seems to follow from predator-avoidance decision making, that is, the scenario in which the prey animal is forced to balance food and predator pressures and decide either to decrease foraging or to risk exposure to predators.5 Both alternatives have high costs and involve high levels of stress, but often animals decrease the likelihood of being caught by choosing to eat less. They tend to hide in places where food is scarce but the presence of predators is less likely. In those conditions, additional stress responses are likely to be triggered by starvation and dehydration. Predation thus is not only the main direct stressor in the wild but is also an indirect cause of stress through the strategies animals adopt to avoid it. This shows how the risk of predation implies continuous suffering for many wild animals.

Wild animals’ suffering is often made worse by certain human interventions in the wild that are carried out for ecological purposes. The most significant example of this is the reintroduction of predators into ecosystems where they have long been extinct. This form of intervention in trophic chains is usually employed in the context of ecosystem restoration programs that aim at reconstructing some aspects of an ecosystem, such as the preservation of a threatened species. This is sometimes done by identifying animals that threaten an ecosystem in some way (e.g. deers “overgraze” some plant species) and reintroducing the animals’ ancient predator (e.g. wolves), aiming to repair the situation. The expected results are: (1) the wolves eat the deers, reducing the number of deers who graze by reducing their population and, more importantly, (2) deers stop grazing out of fear of being preyed on by the wolves. Instead of grazing freely in open areas, deers hide in places where wolves cannot see them easily and eat other, smaller plants. The biological dynamics that result from this have been called the “ecology of fear”.

One of the best known cases of this took place at Yellowstone Park in the USA and it is estimated that since the reintroduction of wolves, deers have decreased to one half of their original population.6 As we have seen above, predator-induced stress can be an extreme cause of suffering for wild animals, both directly and indirectly. Apart from living in a permanent “landscape of fear,” these animals also suffer from scarcity of food and often die from all sorts of associated complications, such as diseases and injuries due to malnutrition.

The stress of social animals

Living in social groups involves costs for animals, primarily due to social conflict and competition. Many social species have dominance hierarchies, and the social status that each animal has in the hierarchy dramatically influences his level of wellbeing. This has shown to be the case particularly with stress-related diseases.7 It has been well documented that social subordination, for example, constitutes a stressor in different social species, such as primates,8 monkeys,9 rodents10 and fishes.11 In low-ranking animals of these social species, depressive responses and a decrease in reproductive competence are often observed.12

Stress due to the adverse effects of maternal separation has been studied in several social species. Maternal separation can be very negative for both mother and infant and have long-lasting influence on their physiology and behavior. After the separation, the mother usually responds by reducing activity, moving with a bent-over body and exhibiting other sickness behaviors induced by the stressful event.13 Infants who are separated from their mothers show increased reactivity to stress throughout their lives and increased risk of disease. This has been observed especially in rodents and primates,14 though other social species are also likely to experience the same effects.


 

Further readings:

Archer, J. E. & Blackman, D. E. (1971) “Prenatal psychological stress and offspring behavior in rats and mice”, Developmental Psychobiology, 4, pp. 193-248.

Biondi, M. & Zannino, L.-G. (1997) “Psychological stress, neuroimmunomodulation, and susceptibility to infectious diseases in animals and man: A review”, Psychotherapy and Psychosomatics, 66, pp. 3-26.

Blanchard, R. J.; Nikulina, J. N.; Sakai, R. R.; McKittrick, C. ; McEwen, B. & Blanchard, D. C. (1998) “Behavioral and endocrine change following chronic predatory stress”, Physiology & Behavior, 63, pp. 561-569.

Boonstra, R.; Hik, D.; Singleton, G. R. & Tinnikov, A. (1998) “The impact of predator-induced stress on the snowshoe hare cycle”, Ecological Monographs, 68, pp. 371-394.

Caso, J. R.; Leza, J. C. & Menchen, L. (2008) “The effects of physical and psychological stress on the gastrointestinal tract: Lessons from animal models”, Current Molecular Medicine, 8, pp. 299-312.

Cohen, S.; Line, S.; Manuck, S. B.; Rabin, B. S.; Heise, E. R. & Kaplan, J. R. (1997) “Chronic social stress, social status, and susceptibility to upper respiratory infections in nonhuman primates”, Psychosomatic Medicine, 59, pp. 213-221.
Creel, S.; Winnie, J. A., Jr. & Christianson, D. (2007) “Predation risk affects reproductive physiology and demography of elk”, Science, 315, pp. 960.

Creel, S.; Winnie, J. A., Jr. & Christianson, D. (2009) “Glucocorticoid stress hormones and the effect of predation risk on elk reproduction”, Proceedings of the National Academy of Sciences of the USA, 106, pp. 12388-12393 [accessed on 8 March 2013].

de Catanzaro, D. (1988) “Effect of predator exposure upon early pregnancy in mice”, Physiology & Behavior, 43, pp. 691-696.

Dwyer, C. M. (2004) “How has the risk of predation shaped the behavioural responses of sheep to fear and distress?”, Animal Welfare, 13 (3), pp. 269-281.

Engh, A. L.; Beehner, J. C.; Bergman, T. J.; Whitten, P. L.; Hoffmeier, R. R.; Seyfarth, R. M. & Cheney, D. L. (2006) “Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus)”, Proceedings of the Royal Society of Biological Sciences, 273, pp. 707-712.

Figueiredo, Helmer F.; Bodie, Bryan L.; Tauchi, Miyuki; Dolgas, C. Mark & Herman, James P. (2003) “Stress integration after acute and chronic predator stress: Differential activation of central stress circuitry and sensitization of the hypothalamo-pituitary-adrenocortical axis”, Endocrinology, 44, pp. 5249-5258.

Fossat, P.; Bacqué-Cazenave, J.; de Deuerwaerdère, P.; Delbecque, J.-P. & Cattaert, D. (2014) “Anxiety-like behavior in crayfish is controlled by serotonin”, Science, 344, pp. 1293-1297.
Galhardo, L. & Oliveira, R. F. (2009) “Psychological stress and welfare in fish”, Annual Review of Biomedical Sciences, 11, pp. 1-20.

Kagawa, N. & Mugiya, Y. (2000) “Exposure of goldfish (Carassius auratus) to bluegills (Lepomis macrochirus) enhances expression of stress protein 70 mRNA in the brains and increases plasma cortisol levels”, Zoological Science, 17, pp. 1061-1066 [accessed on 2 April 2014].

Lazar, N. L.; Neufeld, R. W. J. & Cain, D. P. (2011) “Contribution of nonprimate animal models in understanding the etiology of schizophrenia”, Journal of Psychiatry & Neuroscience, 36, pp. E5-E29 [accessed on 12 June 2014].

Lima, S. L. (1998) “Stress and decision making under the risk of predation: Recent developments from behavioral, reproductive, and ecological perspectives”, Advances in the Study of Behavior, 27, pp. 215-290.

Love, O. P.; McGowan, P. O. & Sheriff, M. J. (2012) “Maternal adversity and ecological stressors in natural populations: the role of stress axis programming in individuals, with implications for populations and communities”, Functional Ecology, 27, pp. 81-92.
Martin, T. E. (2011) “The cost of fear”, Science, 334, pp. 1353-1354.

Mashoodh, R.; Sinal, C. J. & Perrot-Sinal, T. S. (2009) “Predation threat exerts specific effects on rat maternal behaviour and anxiety-related behaviour of male and female offspring”, Physiology & Behavior, 96, pp. 693-702.

McGrady, A. V. (1984) “Effects of psychological stress on male reproduction: A review”, Systems Biology in Reproductive Medicine, 13, pp. 1-7.

Norrdahl, K. & Korpimäki, E. (1998) “Does mobility or sex of voles affect risk of predation by mammalian predators?”, Ecology, 79, pp. 226-232.

Ottenweller, J.E. (2007) “Animal models (non-primate) for human stress”, in Fink, G. (ed.) Encyclopedia of stress, 2nd ed., Amsterdam: Academic Press, pp. 190-195.

Sheriff, M. J.; Krebs, C. J. & Boonstra, R. (2010) “The ghosts of predators past: population cycles and the role of maternal programming under fluctuating predation risk”, Ecology, 91, pp. 2983-2994.

Zanette, Liana Y.; White, Aija F.; Allen, Marek C. & Clinchy, Michael (2011) “Perceived predation risk reduces the number of offspring songbirds produce per year”, Science, 334, pp. 1398-1401.


Notes:

1 Allaby, M. (ed.) (1999) Oxford dictionary of zoology, Oxford: Oxford University Press.
2 See for example, Wiepkema, P. R. & van Adrichem, P. W. M. (eds.) (1987) Biology of stress in farm animals: An integrative approach, Hinglaw: Kluwer Academic Publishers; Moberg, G. P. & Mench, J. A. (2000) The biology of animal stress: Basic principles and implications for animal welfare, New York: Cabi; Broom, D. M. & Johnson, K. G. (1993) Stress and animal welfare, Hinglaw: Kluwer Academic; Dantzer, R. & Mormède, P. (1983) “Stress in farm animals: A need for reevaluation”, Journal Animal Science, 57, pp. 6-18.

3 McCauley, S.; Rowe, J. L. & Fortin, M.-J. (2011) “The deadly effects of ‘nonlethal’ predators”, Ecology, 92, pp. 2043-2048.

4 Gregory, N. G. (2004) Physiology and Behaviour of Animal Suffering, Oxford: Blackwell Science, p. 18.

5 Clinchy, M.; Zanette, L.; Boonstra, R.; Wingfield, J. C. & Smith, J. N. M. (2004) “Balancing food and predator pressure induces chronic stress in songbirds”, The Royal Society, 271, pp. 2473-2479, [accessed on 5 January 2013].

6 Horta, O. (2010) “The ethics of the ecology of fear against the nonspeciesist paradigm: A shift in the aims of intervention in nature”, Between the Species, 13 (10) [accessed on 17 January 2013].

7 Sapolsky, R. M. (2004) “Social status and health in humans and other animals”, Annual Review of Anthropology, 33, pp. 393-418 [accessed on 23 September 2013].
8 Abbott, D. H; Keverne, E. B.; Bercovitch, F. B.; Shively, C. A.; Mendoza, S. P.; Saltzman, W.; Snowdon, C. T.; Ziegler, T. E.; Banjevic, M.; Garland, T., Jr. & Sapolsky, R. M. (2003) “Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates”, Hormones and Behavior, 43, pp. 67-82.

9 Shiverly, C. A.; Laber-Laird, K. & Anton, R. F. (1997) “Behavior and physiology of social stress and depression in female cynomolgus monkeys”, Biological Psychiatry, 41, pp. 871-882.

10 Koolhas, J. M.; De Boer, S. F.; De Rutter, A. J.; Meerlo, P., Sgoifo A. (1997) “Social Stress in Rats and Mice”, Acta Physiol Scand Suppl , 640, pp. 69-72; Koolhas, J. M.; De Boer, S. F.; Meerlo P.; Strubbe, J. H. & Bohus, B. (1997) “The temporal dynamics of the stress response”, Neuroscience and Biobehavioral Reviews, 21, pp. 775-782.

11Fox, H. E.; White, S. A.; Kao, M. H. & Russell, D. F. (1997) “Stress and dominance in a social fish”, The Journal of Neuroscience, 17, pp. 6463-6469.
12 Sapolsky, R. M. (2005) “The influence of social hierarchy on primate health”, Science, 308, pp. 648-652.
13 Hennessy, M. B.; Deak, T. & Schiml-Webb, P. A. (2001) “Stress-induced sickness behaviors: An alternative hypothesis for responses during maternal separation”, Developmental Psychobiology, 39, pp. 76-83.
14 Pryce, C. R.; Rüedi-Bettschen, D.; Dettling, A. C. & Feldon, J. (2002) “Early life stress: long-term physiological impact in rodents and primates”, News in Physiological Sciences, 17, pp. 150-155.

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