Psychological stress in wild animals

Psychological stress in wild animals

This text is part of a series examining the conditions of animals living in the wild. For more texts examining the ways animals in the wild suffer and die, see our main page on the situation of animals in the wild. For information on how we can help animals, see our section on helping animals in the wild.

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 heart rate and blood pressure and suppression of the immune system, among ­­­­­other negative health effects. It can lead to fatal arrhythmias or heart attacks.2

While the effects of stress in domestic animals have been well documented,3 there have been fewer studies on wild animals, and the severity and number of stressors that afflict wild animals have probably been underestimated by scientific research, except for the effects of captivity on wild animals. Wild animals have to face adverse circumstances on a daily basis that are usually stressful: physical trauma, disease, food shortages, conflicts with others of their species or herd, and molting,4 among other circumstances. Here we will cover stress related to predation and social living.

Predator-induced stress seems to arise in two major ways. The first is directly from the predatory pursuit itself, in which animals must face the stress of fleeing or fighting. The confrontation may be so intense that the prey animal dies of stress.5 Wild rats have died of heart attacks after being forced to listen to a tape recording of a cat-rat fight,6 and black-capped chickadees who were forced to listen to the sounds of a predator exhibited long-term stress responses similar to PTSD.7

Second, stress in terrestrial and aquatic animals seems to follow indirectly from predator-avoidance decision making, that is, a scenario in which the prey animal is forced to balance food and predator pressures and decide either to decrease foraging or to risk greater exposure to predators.8 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 the presence of predators is less likely but food is scarce. In those conditions, additional stress responses are likely to be triggered by starvation and dehydration. Predation thus is not only a 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 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 whose activities change an ecosystem in some way (e.g. deer populations “overgraze” some plant species) and reintroducing the animals’ ancient predator (e.g. wolves), in an attempt to prevent them from eating certain foods. The expected results are: (1) the wolves reduce their population sizes by eating them and (2) an even bigger impact when deer populations stop grazing out of fear of being preyed upon by the wolves. Instead of grazing freely in open areas, they hide in places where wolves cannot see them easily, and eat other, less plentiful and less nutritious plants. The biological dynamics that result from this is called the “ecology of fear”.

One of the best known cases of this took place in Yellowstone Park in the USA. As we have seen above, predator-induced stress can be a cause of extreme 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 associated complications, such as diseases and injuries due to malnutrition. It is estimated that since the reintroduction of wolves, the deer population in Yellowstone has decreased to one half of its original size.9

New environments

Animals may become stressed when they are forced into a new area. They might have to move because of severe weather conditions, lack of food, fires, and natural disasters. For many animals, it takes generations to learn about their new environment and transmit knowledge to younger generations. While they are adjusting, they can face starvation and the stress of trying to learn to live and find food in unfamiliar surroundings.

Frightening sounds

Animals, especially young animals who have not learned about their environment yet, can be frightened by loud and unfamiliar sounds made by other animals, approaching storms, airplanes, or drones.10 Many animals are affected by fear-inducing sounds that are made intentionally by other animals in order to scare them away from food or mates.

Some birds intentionally mimic the warning calls of other birds in order to deceive them. African fork-tailed drongos can mimic a wide variety of warning calls, not only of other birds but also of some mammals such as meercats. In response to the warnings, the animals flee from their food supplies, and the drongos swoop in to eat the abandoned food. This can cause the victims of the false alarms not only the stress of responding to a non-existent danger, but also from lost food. They are then forced to find new food, which itself can be a risky and stressful event. Victims of this deception reduce their response to repeated false alarms, but drongos are able to keep the fear response high by varying the types of alarm calls they make. Some birds continue to live with drongos even after they appear to understand the drongos’ tricks. They may tolerate the added stress because the genuine anti-predator calls of the drongos provide some protection.11

Primates also use this kind of deception. For example, lower status tufted capuchin monkeys make false warning calls when higher status monkeys are eating, presumably in order to get a chance to eat without being bullied or attacked. They give these false calls more often when there is a type of highly-contested food like bananas that is being monopolized by more dominant monkeys.12

It’s common for males to guard females after mating. This is seen in animals from crickets to magpies to baboons. Some animals, like squirrels and swallows, use false warning calls after mating, in order to scare potential competitors away or to prevent their partners from leaving them.13

The stress of social animals

Living in social groups involves costs for animals, primarily due to social conflict and competition. Many species of animals that are social and subsocial (such as crickets and lobsters) have dominance hierarchies.14 Although a lot of fighting for position is ritualized, some involves actual violence or ongoing harassment. The social status that each animal has in the hierarchy dramatically influences her level of wellbeing, particularly when it comes to stress-related diseases.15 It has been well documented that social subordination, for example, constitutes a stressor in different social species, such as primates,16 rodents17 and fishes.18 In low-ranking animals of these social species, depressive responses and a decrease in reproductive opportunities are often observed.19

In some cases, animals are shunned20 or excluded21 from their groups. An animal may be forced out because of antisocial behavior, being regarded as a threat to a dominant male or female, or being considered harmful or useless to the group due to illness or frailty. When food or other resources are scarce, more aggressive animals may force some of the animals to leave. Animals forced out of a group will be at greater risk of predation and starvation and may suffer additional stress from lack of social interaction.

Other subordinate animals may face frequent threats and intimidation in order to remain in their group. Common causes of intimidation are over food access and sexual competition, often together because of the extra energy demands of reproduction. Dominant males might attack or threaten other males who try to mate, and kill children who have other fathers, causing grief to the mothers, who are then coerced into mating with them. You can learn more about this in our pages about intraspecific conflict and sexual conflict.

Subordinate females can face constant threats and deprivation in matrilineal groups, in which dominant females use aggression and intimidation to limit the access of subordinates to mating opportunities and food.22 The children of subordinate females might also be killed by the dominant female. She may force the subordinates to serve her, especially to further her reproductive success. This is common in meerkats. The mothers whose children were killed must help care for the young of the dominant female or else be evicted from their colony and face the hazards of trying to survive on their own.23

Stress due to the adverse effects of maternal separation has been studied in numerous social species. Maternal separation can have a long-lasting effect on the physiology and behavior of both mother and child. After separation, the mother usually responds by reducing activity, moving with a bent-over body, and exhibiting other sickness behaviors induced by the stressful event.24 Infants who are separated from their mothers have increased risk of disease and show increased reactivity to stress throughout their lives. In wild animals, this has been observed in cetaceans, elephants, rodents and primates,25 though other social species are also likely to experience the same effects. Animals who receive parental care when they are young but live solitary lives as adults can also suffer lasting effects from maternal separation.26


Penguin parents responding to the death of their child

In addition to the effects of maternal separation, there are many documented cases of elephants, cetaceans, dogs, birds, and other animals27 exhibiting grieving behaviors at the loss of family members or friends.


Elephants responding to the death of a matriarch


Funeral procession for baby elephant


Animals mourn the loss of family and friends

In mammals, birds, and arthropods, there is evidence of animals showing PTSD-like symptoms in response to stressful events, of mood and anxiety disorders, and of negative moods spreading within social groups.28 In some species, like rabbits and squirrels, living in a state of chronic stress appears to be an adaptive response to environmental threats.29

Psychological stress, whether acute or chronic, negatively affects the wellbeing of animals. Sometimes it is adaptive and improves and animal’s ability to survive at the expense of their psychological wellbeing. In other cases, it can impair an animal’s ability to function and increase their risk of multiple threats to their health and safety. Although it is less widespread than other sources of suffering, it can be debilitating and life-threating to those who suffer from it.


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.

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

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].

Dwyer, C. M. (2004) “How has the risk of predation shaped the behavioural responses of sheep to fear and distress?”, Animal Welfare, 13, 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, M. (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 Alkema, M. (2019) “How stress can weaken defenses: How the ‘fight-or-flight’ response impairs cellular defense mechanisms”, ScienceDaily, 9 September [accessed on 24 September 2019]. Aydinonat, D.; Penn, D. J.; Smith, S.; Moodley, Y.; Hoelzl, F.; Knauer, F. & Schwarzenberger, F. (2014) “Social isolation shortens telomeres in African Grey Parrots (Psittacus erithacus erithacus)”, 9 (4) [accessed on 26 September 2019]. Heimbürge, S.; Kanitz, E. & Otten, W. (2019) “The use of hair cortisol for the assessment of stress in animals”, General and Comparative Endocrinology, 270, pp. 10-17. Bayazit, V. (2009) “Evaluation of cortisol and stress in captive animals”, Australian Journal of Basic and Applied Sciences, 3, pp. 1022-1031. Richter, V. & Freegard, C. (2009) First aid for animals, Canberra: Department of Environment and Conservation [accessed on 24 September 2019].

3 See for example: Wiepkema, P. R. & Adrichem, P. W. M. van (eds.) (1987) Biology of stress in farm animals: An integrative approach, Hinglaw: Kluwer Academic; 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, Dordrecht: Kluwer Academic; Dantzer, R. & Mormède, P. (1983) “Stress in farm animals: A need for reevaluation”, Journal of Animal Science, 57, pp. 6-18; Bethell, E. J. (2015) “A ‘how-to’ guide for designing judgment bias studies to assess captive animal welfare”, Journal of Applied Animal Welfare Science, 18 (sup. 1), pp. S18-S42.

Examples of studies on the effects of stress on invertebrates are anxiety during molting, social isolation as a cause of stress and aggression in spiders, and pessimism in bees under stress: Bacqué-Cazenave, J.; Berthomieu, M.; Cattaert, D.; Fossat, P.; Delbecque, J. P. (2019) “Do arthropods feel anxious during molts?”, Journal of Experimental Biology, 222 [accessed on 24 September 2019]; Chiara, V.; Portugal, F. R. & Jeanson, R. (2019) “Social intolerance is a consequence, not a cause, of dispersal in spiders”, PLOS Biology, 17 (7) [accessed on 22 November 2019]; Mendl, M.; Paul, E. S. & Chittka, L. (2011) “Animal behaviour: Emotion in invertebrates?”, Current Biology, 21, pp. R463-R465 [accessed on 24 September 2019].

4 Bacqué-Cazenave, J.; Berthomieu, B.; Cattaert , D.; Fossat , P. & Delbecque, J. P. (2019) “Do arthropods feel anxious during molts?”, op. cit.

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

6 Gregory, N. G. (2004) Physiology and behaviour of animal suffering, Oxford: Blackwell Science, p. 18.

7 Zanette, L. Y; Hobbs, E. C.; Witterick, L. E.; MacDougall-Shackleton, S. A. & Clinchy, M. (2019) “Predator-induced fear causes PTSD-like changes in the brains and behaviour of wild animals”, Scientific Reports, 9 [accessed on 24 September 2019].

8 Cherry, M. J.; Warren, R. J. & Conner, L. M. (2019) “Fire‐mediated foraging tradeoffs in white‐tailed deer”, Ecosphere, 8 (4) [accessed on 9 September 2019]. Clinchy, M.; Zanette, L.; Boonstra, R.; Wingfield, J. C. & Smith, J. N. (2004) “Balancing food and predator pressure induces chronic stress in songbirds”, Proceedings of the Royal Society B: Biological Sciences, 271, pp. 2473-2479 [accessed on 5 January 2013]. Preisser, E. L.; Bolnick, D. I. & Benard, M. F. (2005) “Scared to death? The effects of intimidation and consumption in predator–prey interactions”, Ecological Society of America, 86, pp. 501-509.

9 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].

10 Wegdell, F.; Hammerschmidt, K. & Fischer, J. (2019) “Conserved alarm calls but rapid auditory learning in monkey responses to novel flying objects”, Nature Ecology & Evolution, 3, pp. 1039-1042.

11 Flower, T. P.; Gribble, M. & Ridley, A. R. (2014) “Deception by flexible alarm mimicry in an African Bird”, Science, 344, pp. 513-516.

12 Wheeler, B. C. (2009) “Monkeys crying wolf? Tufted capuchin monkeys use anti-predator calls to usurp resources from conspecifics”, Proceedings of the Royal Society B: Biological sciences, 276, pp. 3013-3018.

13 Tamura, N. (1995) “Postcopulatory mate guarding by vocalization in the Formosan squirrel”, Behavioral Ecology and Sociobiology, 36, pp. 377-386. Møller, A. P. (1990) “Deceptive use of alarm calls by male swallows, Hirundo rustica: a new paternity guard”, Behavioral Ecology, 1, pp. 1-6.

14 On dominance hierarchies in crickets, see: Rudin, F. S.; Tomkins, J. L. & Simmons, L. W. (2017) “Changes in dominance status erode personality and behavioral syndromes”, Behavioral Ecology, 28, pp. 270-279 [accessed on 26 September 2019]. There are also dominance hierarchies in some subsocial and solitary animals like lobsters and octopuses, primarily over shelter, territory, and food. See Cigliano, J. (1993) “Dominance hierarchies in octopuses: Serotonin”, Animal Behaviour, 46, pp. 677-684; Cigliano, J. (1991) “Dominance and den use in Octopus bimaculoides”, Animal Behaviour, 46, pp. 677-684; Sato, D. & Nagayama, T. (2012) “Development of agonistic encounters in dominance hierarchy formation in juvenile crayfish”, Journal of Experimental Biology, 215, pp. 1210-1217 [accessed on 20 December 2019]; Huber, R.; Smith, K.; Delago, A.; Isaksson, K. & Kravitz, E. A. (1997) “Serotonin and aggressive motivation in crustaceans: Altering the decision to retreat”, Proceedings of the National Academy of Science of the United States of America, 94, pp. 5939-5942 [accessed on 25 September 2019]; Sbragaglia, V.; Leiva, D.; Arias, A.; García, J. A.; Aguzzi, J. & Breithaupt, T. (2017) “Fighting over burrows: The emergence of dominance hierarchies in the Norway lobster (Nephrops norvegicus)”, Journal of Experimental Biology, 220, pp. 4624-4633 [accessed on 26 September 2019].

15 Sapolsky, R. M. (2004) “Social status and health in humans and other animals”, Annual Review of Anthropology, 33, pp. 393-418.

16 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. 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.

17 Koolhas, J. M.; de Boer, S. F.; de Rutter, A. J.; Meerlo, P. & Sgoifo A. (1997) “Social stress in rats and mice”, Acta Physiologica Scandinavica. Supplementum, 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.

18 Bacqué-Cazenave, J.; Cattaert, D.; Delbecque, J.-P. & Fossat, P. (2017) “Social harassment induces anxiety-like behaviour in crayfish”, Scientific Reports, 7 [accessed on 25 September 2019]. Fox, 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 [accessed on 20 December 2019].

19 Sapolsky, R. M. (2005) “The influence of social hierarchy on primate health”, Science, 308, pp. 648-652.

20 Castro, J. (2013) “Monkeys shun selfish others”, Live Science, March 05 [accessed on 26 September 2019]. Massen, J. J. M.; Ritter, C. & Bugnyar, T. (2015) “Tolerance and reward equity predict cooperation in ravens (Corvus corax)”, Scientific Reports, 5 [accessed on 26 September 2019].

21 Thompson, F. J.; Cant, M. A.; Marshall, H. H.; Vitikainen, E. I. K.; Sanderson, J. L.; Nichols, H. J.; Gilchrist, J. S.; Bell, M. B. V.; Young, A. J.; Hodge, S. J. & Johnstone, R. A. (2017) “Explaining negative kin discrimination in a cooperative mammal society”, Proceedings on the National Academy of Sciences, 114, pp. 5207-5212 [accessed on 26 September 2019].

22 Clutton-Brock, T. H. & Huchard, E. (2013) Social competition and its consequences in female mammals”, Journal of Zoology, 289, pp. 151-171 [accessed on 26 September 2019].

23 MacLeod, K. J.; Nielsen, J. F. & Clutton-Brock, T. H. (2013) “Factors predicting the frequency, likelihood and duration of allonursing in the cooperatively breeding meerkat”, Animal Behaviour, 86, pp. 1059-1067. Stephens, P. A.; Russell, A. F.; Young, A. J.; Sutherland, W. J. & Clutton-Brock, T. H. (2015) “Dispersal, eviction, and conflict in meerkats (Suricata suricatta): An evolutionarily stable strategy model”, American Naturalist, 165, pp. 120-135.

24 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.

25 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. Vetulani, J. (2013) “Early maternal separation: A rodent model of depression and a prevailing human condition”, Pharmacological Reports, 65, pp. 1451-1461.

26 Patoka, J.; Kalous, L. & Bartoš, L. (2019) “Early ontogeny social deprivation modifies future agonistic behaviour in crayfish”, Scientific Reports, 9 [accessed on 8 January 2019].

27 Yeoman, B. (2018) “When animals grieve”, The National Wildlife Federation, Jan 30 [accessed on 25 September 2019]. Plotnik, J. M. & de Waal, F. B. M. (2014) “Asian elephants (Elephas maximus) reassure others in distress”, PeerJ, 2 [accessed on 3 December 2019].

28 Noguera, J. C.; Kim, S.-J. & Velando, A (2017) “Family-transmitted stress in a wild bird”, Proceedings on the National Academy of Sciences of the United States of America, 114, pp. 6794-6799 [accessed on 18 December 2019]. Adriaense, J. E. C.; Martin, J. S.; Schiestl, M.; Lamm, C. & Bugnyar, T. (2019) “Negative emotional contagion and cognitive bias in common ravens (Corvus corax)”, Proceedings of the National Academy of Sciences of the United States of America, 116, pp. 11547-11552 [accessed on 26 September 2019]. Bekoff, M. (2011) “Grief, mourning, and broken hearted animals,” Psychology Today, 26 November [accessed on 24 September 2019]. Chiara, V.; Portugal, F. R. & Jeanson, R. (2019) “Social intolerance is a consequence, not a cause, of dispersal in spidersPLOS Biology, 17 (7) [accessed on 22 December 2019]. Ferdowsian, H. R.; Durham, D. L.; Kimwele, C.; Kranendonk, G.; Otali, E.; Akugizibwe, T.; Mulcahy, J. B.; Ajarova, L. & Johnson, C. M. (2011) “Signs of mood and anxiety disorders in chimpanzeesPLOS ONE, 6 (6) [accessed on 26 September 2019].

29 Boonstra, R. (2012) “Reality as the leading cause of stress: Rethinking the impact of chronic stress in nature”, Functional Ecology, 27, pp. 11-23 [accessed on 2 December 2019].