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Fight or Flight Responses
Fight or Flight Responses L. M. Romero, Tufts University, Medford, MA, USA ã 2010 Elsevier Ltd. All rights reserved.
Introduction When animals are faced with perceived or anticipated dangers from the environment, they initiate a stress response – a generic term for a bewildering suite of physiological and behavioral responses that are designed to help an animal survive these dangers (called stressors because they elicit a stress response). The two best-studied physiological responses are the release of glucocorticoid steroid hormones and the activation of the sympathetic nervous system. Discussion of the glucocorticoid response is presented in other articles and sympathetic activation, usually referred to as the fight-or-flight response, is the subject of this article. The term fight-or-flight dates back to the early twentieth century and is an excellent brief description of the role of sympathetic nervous system activation. Fight-orflight evokes immediacy. Life is hanging in the balance and there is no time for reproduction, mate selection, foraging, digestion, etc. At this precise instant, only survival is important. The fight-or-flight response is the firstline physiological mechanism for giving an animal its best chance for survival. If an animal mounts a fight-or-flight response, it suggests that the animal is reacting quickly, strongly, and immediately in order to survive. The sympathetic nervous system mediates these reactions. Although many stressors can elicit a fight-or-flight response, the stressor most commonly associated with a fight-or-flight response is a predator attack. Predators can have numerous behavioral effects on their prey, including increasing vigilance, decreasing foraging times, changing how animals interact with other individuals (such as flocking or forming herds), and even altering where individual animals choose to live (i.e., changing prey distribution patterns). Predator presence, predator calls, and predator odors can all evoke a fight-or-flight response and even the threat of predation is sufficiently powerful that animals often react as if there were predators present even when there are none. These predator-induced changes in behavior have been studied for decades, but predator pressure can also change hormonal and physiological systems. Predation risk alters the hormonal and physiological regulation of reproduction and appears to have led to the evolution, in some bird species, of the restriction of sleep to one hemisphere of the brain at a time, an adaptation thought to allow the bird to maintain vigilance for predators at all times. The physiological changes associated with predation risk are so powerful that chronic
710
exposure to predator cues is used as a laboratory model for studying human anxiety. Clearly, the fight-or-flight response occupies a critical position in coping with a short-term stressor such as a predator attack. This article presents an overview of how the sympathetic nervous system regulates a fight-or-flight response and how that response might help an animal to survive.
Sympathetic Nervous System The details of sympathetic activation are highly conserved among vertebrates. Although there are some species differences, the broad outlines are present in every species examined, from fish to mammals. This should highlight how central the fight-or-flight response is for survival. Catecholamines The activity of the sympathetic nervous system is primarily regulated by a class of hormones called catecholamines. Epinephrine and norepinephrine are the two primary catecholamines involved in the fight-or-flight response. They are equivalent to adrenaline and noradrenaline, epinephrine/norepinephrine being the names used in the United States and adrenaline/noradrenaline used in Europe. Epinephrine and norepinephrine are produced primarily in neurons (or modified neurons in the case of adrenal tissue). Synthesis begins with the amino acid tyrosine and ends with the rate-limiting conversion to norepinephrine by tyrosine hydroxylase. Epinephrine can then be converted from norepinephrine, using the enzyme phenylethanolamine N-methyltransferase (PNMT). PNMT is then the rate-limiting enzyme for epinephrine production. Both tyrosine hydroxylase and PNMT are often the targets for assays and in situ localizations to determine where, and potentially how much, epinephrine and norepinephrine are being produced. Anatomy The location of epinephrine release depends in part on the species. In mammals, epinephrine is primarily produced in the adrenal medulla – the center portion of the adrenal gland. The adrenal medulla is essentially a modified sympathetic ganglion where each secretory cell
Fight or Flight Responses
is a neuron without an axon. Epinephrine and norepinephrine are released from two different cell populations in the adrenal medulla. Another major source of norepinephrine is nerve terminals of the sympathetic nervous system. Most nonmammalian species, however, lack a well-defined adrenal medulla. In these species, cells that release epinephrine and norepinephrine are embedded in the wall of the kidneys. These cells are called chromaffin and are homologous to cells in the adrenal medulla of mammals. The physiological responses in mammals and nonmammals, however, appear to be essentially identical. When a stressor begins, epinephrine and norepinephrine are released from the adrenal medulla and norepinephrine is released from the sympathetic nerve terminals. Because the secretory cells are neurons, catecholamine release is very quick and effects can be seen in less than a second. Catecholamines orchestrate the entire fight-or-flight response. The amount released, however, is very important. Sympathetic activation is not an all-or-nothing response and the strength of the response can be modulated to the needs of the moment. If too little response is released, the impact on target tissues will be insufficient; too much release, however, is often fatal. Consequently, the amount of epinephrine and norepinephrine released is usually carefully titrated to correspond to the severity of the stressor. Physiological Effects Once released, the catecholamines exert a number of effects throughout the body. Catecholamine-induced changes in the cardiovascular system have been known for almost a century. Catecholamines alter the delivery of nutrients, especially glucose and oxygen, to the brain, heart, lungs, and skeletal muscles, at the cost of the peripheral tissues. They do this by increasing cardiac output, increasing blood pressure, vasodilating arteries in skeletal muscle, vasoconstricting arteries in the kidney, gut, and skin, vasoconstricting veins in general, stimulating the lungs to dilate air passages, and initiating hyperventilation. Although it might seem counterintuitive that catecholamines would exert such opposite effects as both vasodilation and vasoconstriction, the explanation resides in a difference in receptors. Catecholamine receptors come in both a- and b-varieties, both of which have two subforms (a1 and a2, b1 and b2). The a-receptors have higher affinity for norepinephrine, whereas the b-receptors have a higher affinity for ephinephrine. Furthermore, each receptor type mediates different functions. For example, in arteries a1-receptors mediate vasoconstriction, whereas b2-receptors mediate vasodilation. However, the binding dynamics of a- and b-receptors described earlier apply to mammals. Birds have different
711
binding dynamics (both epinephrine and norepinephine bind preferentially to b-receptors) and other taxa may show slight differences as well. Consequently, the physiology of catecholamine function can be richly varied in different species. A second major effect of catecholamines is to increase the energy available to the muscles and brain, especially when glucose is being rapidly consumed during a fight or when fleeing. Catecholamines accomplish this by stimulating the liver to increase the production of glucose, specifically via glycogen breakdown, which is then released for delivery to peripheral tissues. The end result is a quick burst of glucose that can be used by muscles, the brain, and other essential tissues. Catecholamines also stimulate white adipose tissue to release free fatty acids that the liver can then use to produce more glucose. Once extra glucose becomes available in the blood stream, the final step in this process is to get the glucose into the cells that need it. Catecholamines also stimulate increased glucose uptake in these cells. A third major effect of catecholamines is to regulate a number of effects in the skin. Catecholamines vasoconstrict blood vessels in the skin in order to shunt blood preferentially to internal organs, stimulate sweat production, and induce piloerection, the standing up of hairs in their follicles. Piloerection may serve two purposes: to enhance heat retention and to make the animal appear larger and fiercer to rivals and predators. Catecholamines may also regulate facultative changes in skin color in some species, especially to hide from predators. Finally, the nervous system is also a major target for catecholamines. Their major effects in the brain are to increase attention and alertness. This leads to increased performance on cognitive tasks as well as a decrease in muscular and psychological fatigue. Catecholamines also cause the pupils to dilate, which aids in distance vision.
Increases in Heart Rate Measuring the strength of the fight-or-flight response or even determining whether a fight-or-flight response is initiated, is often difficult. One problem is how fast the sympathetic nervous system is activated. Catecholamines are released into the blood so quickly that it is virtually instantaneous. Currently, one of the few techniques available is to measure changes in heart rate as an index of catecholamine release. Basic regulation of cardiac function is common across the vertebrates with epinephrine as the primary mediator of heart rate during exposure to a stressor. Epinephrine is released either directly from nerve terminals or indirectly from the adrenal and binds to b-receptors on the heart. Epinephrine results in an increase in heart rate (tachycardia) after most stressors. Furthermore, the degree of tachycardia depends upon the
712
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strength of the stressor – stronger stressors evoke higher increases in heart rate. The diversity of stressors that can elicit tachycardia is impressive. Much of the work has been done under laboratory conditions, where stressors such as sounds, lighting conditions, novel odors, confinement, and abnormal social groups can stimulate increases in heart rate. In addition, a small but growing number of studies indicate that wild free-living animals increase heart rate in response to stressors such as human disturbance, social interactions, and capture and handling. Social interactions are potent stressors that can result in robust tachycardia. However, animals can modulate these responses. For example, animals can habituate to intermittent social stressors, resulting over time in lower responses to equivalent social situations. Only the animal that wins the social encounter habituates, however. The loser retains, and even augments, its original tachycardia during subsequent encounters. In addition, the degree of tachycardia in the loser can depend upon the individual coping style of the animal. Animals have been shown to have either reactive or proactive coping styles when faced with novel situations. When faced with many, but not all, stressors, animals with reactive coping styles show a stronger activation of the sympathetic nervous system and thus a stronger tachycardia. Although stressors induce tachycardia, the relationship can be reversed experimentally. The degree of tachycardia can be used to infer the strength of a stressor. If a stimulus evokes tachycardia, it is assumed to be a stressor, and if stressor evokes greater tachycardia than another stressor, then the stressor associated with the greater tachycardia is assumed to be the stronger stressor. There are several examples of this type of work. First, increased crowding evokes greater tachycardia, with the subsequent inference that crowding is stressful to these species. Second, increases in heart rate have also been used to show that many species can distinguish between familiar and unfamiliar conspecific calls, suggesting that vocalizations from neighbors are less stressful than vocalizations from strangers. Finally, animals can have robust increases in heart rate by simply watching agonistic interactions by other animals, even though they are not directly involved. This bystander effect suggests that social interactions, even those in which the individual is not directly involved, can elicit far more robust responses than other potentially dangerous stimuli. In fact, tachycardia can be a more sensitive index of a fight-or-flight response than behavior. Animals often use behavior in order to avoid a costly physiological response – in other words, to avoid a fight-or-flight response. The result is that behavioral and physiological responses are often uncoupled. For example, an animal moving away from a disturbance will not necessarily be in the midst of a fight-or-flight response. In fact, it may be moving away
specifically to avoid a potential stressor. Conversely, a number of studies have indicated that tachycardia can show a strong increase without any overt behavioral changes. Birds sitting in a nest, for example, may be acutely aware of a nearby predator, and show marked tachycardia, even though there is no outward change in behavior. Consequently, increases in heart rate are often better indicators of an underlying physiological fight-orflight response than overt changes in behavior. Heart rate can also be used to determine whether freeliving wild animals are affected by putative anthropogenic stressors. Many things that humans do, such as building roads, ecotourism, wilderness sports, etc., are presumed to serve as potent stressors to wildlife. However, this assumption is rarely tested. Even if these activities change a species’ settlement patterns or reproductive success, it is not necessarily true that the activities will induce a physiological fight-or-flight response. Implanted or attached heart rate transmitters, devices that collect heart rate data from freely behaving animals and transmit those data to a remote detection device, can be used to determine whether anthropogenic activities are, in fact, stressors. The evidence to date suggests that the impact of anthropogenic disturbances is more complex than originally thought. Many anthropogenic disturbances elicit robust fight-or-flight responses and thus can clearly be described as stressors, but other disturbances do not. The presence or absence of a fight-or-flight response may be an excellent diagnostic tool to determine what is, or is not, a stressor. Finally, it should be remembered that an increase in heart rate, driven by the sympathetic nervous system, can extract a heavy price. For many years we have known that humans can go into sudden cardiac arrest and die because of severe emotional trauma. Although it is unknown whether this occurs in wild animals, it could be the mechanism underlying reports of trap death where wild animals spontaneously die for no apparent reason when captured. The fight-or-flight response is clearly necessary to escape from predators, but the increase in heart rate can create its own problems.
Decreases in Heart Rate The uncoupling of tachycardia and behavior points out a weakness of the term fight-or-flight. Not all immediate emergency behaviors can be easily categorized as a fight response or a flight response. Flight generally evokes images of animals running/flying away from a predator. However, moving toward a predator may be a better strategy. Several studies indicate that moving toward an attacking predator, thereby reducing the predator’s maneuvering time, can actually decrease predator success. In fact, often the most effective tactic is to freeze and not
Fight or Flight Responses
move at all: a tactic taken to its extreme in those species that feign death. Furthermore, the type of tactic employed often varies, both between individuals and within the same individual over time. Sometimes the individual flees and sometimes it freezes. These behaviors, freezing or moving towards a predator, are not generally considered to be part of the fight-or-flight response, yet are likely regulated by the same mechanisms. Whether an animal flees or freezes when faced with a predator is not always predictable, but the choices are mutually exclusive with respective pluses and minuses. Fleeing immediately is the better choice when there is sufficient distance and speed to outrun the predator. The downside is that the animal also draws the predator’s attention immediately and almost guarantees a chase. Freezing, on the other hand, may allow the animal to elude detection. This response is especially useful if the animal is not yet detected or has an asset, such as nearby young, that needs to stay hidden. The downside of this choice is that it can allow a predator to get lethally close. The decision whether to freeze or flee is complex, partially dependent upon the individual animal’s predilection, its distance to a refuge, and the potential benefit of confusing a predator by being unpredictable. When an animal chooses to freeze, however, there is a very different change in the sympathetic nervous system. In general, the response is bradycardia, not tachycardia. A classic example is the feigned death of species like the opossum. When faced with a predator, the animal will become limp and nonresponsive to poking and prodding. This behavioral response is accompanied by a marked bradycardia. Heart rate plummets regardless of the behavior of the predator. Bradycardia makes sense in this context – if the goal is to appear dead, then decreasing heart rate helps to damp any behavioral and/or physiological responses. Once the danger has passed, however, the classic sympathetic response resumes and a strong tachycardia ensues. Interestingly, freezing behavior is rarely, if ever, seen in captive animals. Sympathetic activation, with its associated tachycardia, appears to be the default response. Freezing, with its attendant bradycardia, appears to require a specific context that is absent in caged animals.
Seasonal Differences in the Fight-orFlight Response All animals seasonally adjust behavioral and physiological responses. Cardiovascular function and the underlying fight-or-flight response is no exception. For example, resting heart rate is lower during the winter than during the summer for many species. In general, seasonal changes are linked to a lower energetic demand resulting from a lower winter metabolism. However, there are also seasonal differences in sympathetic activation in response to a
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stressor. The fight-or-flight response can be modulated depending upon the life-history stage. For example, animals can show a stronger fight-or-flight response to conspecific crowding when they are defending territories in the spring than when they are gregarious in the winter. The fight- or flight response can also be modulated depending upon the physiological state of the animal. When an animal is in a particularly energy-intensive period, such as molt or pregnancy, the fight- or flight response can be dramatically suppressed. The lack of response highlights that the magnitude, and perhaps even the presence, of a fight-or-flight response may depend upon the season and/ or physiological state of the animal. Seasonal and life-history-stage differences in the fight-orflight response are not well studied. However, understanding how and when sympathetic responses are modulated should provide important insights into the survival benefits of the generalized fight-or-flight response. The modulation of sympathetic activation may be related to seasonal changes in the prevalence and severity of stressors. The end result would be an animal fine-tuning its fight-or-flight response in order to maximize effectiveness.
Sympathetic Responses During Chronic Stress The fight-or-flight response seems well-suited to help an animal cope with short-term emergency situations. If a stressor continues for a long time, however, or if a series of short-term stressors continues in rapid succession, many of the short-term emergency responses can themselves become damaging. When this occurs, it is called chronic stress. The constant and/or repeated initiation of the fight-or-flight response can lead to profound disruption of the sympathetic nervous system. For example, chronic stress can lead to coronary heart disease in both humans and animals. Many studies indicate that, over time, chronic stress leads to a lowering of the magnitude of heart rate elevations in response to a variety of stressors. In other words, chronic stress leads to a damping of the fight-or-flight response. The chronically stressed animal can no longer mount a robust sympathetic response to a novel stressor. This decrease is often interpreted as habituation to the stressor, but other data suggest that this might be too simple an explanation. Stores of both epinephrine and norepinephrine are depleted during chronic stress, which results in diminished release of both hormones. This appears to be the underlying mechanism that results in the attenuated fight-or-flight response. If the fight-or-flight response is indeed down-regulated during chronic stress, it would have tremendous fitness implications. An appropriate fight-or-flight response, necessary to survive stressors in the wild, would be compromised. This suggests that chronic stress greatly impacts on
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Fight or Flight Responses
an animal’s potential survival, especially in terms of evading predators. In contrast, other studies show long-term increases in heart rate during chronic stress. The increase is in both basal heart rates, indicating chronic sympathetic overstimulation, and in the heart rate response to a stressor, that is the fight-or-flight response. The underlying mechanism appears to be increased synthesis and storage of catecholamines, which may allow the animal to respond stronger to a novel stressor. Note that the two sets of studies come to completely opposite results. One set shows a decrease in catecholamines, leading to decreases in the fight-or-flight response, and the other set shows an increase in catecholamines, leading to increases in the fight-or-flight response. The reasons for this disparity are currently unknown, but a difference in individual coping styles is one candidate. The impact of heart rate changes during chronic stress could also be ameliorated over the course of the day. In some models of chronic stress, the heart rates recover quickly once the chronic stress ends. This suggests that the chronic stress-induced changes are not long-lasting. Furthermore, most chronic stress models apply stressors only during a portion of the 24 h cycle (e.g., during the active period). The heart rate can often recover and even overcompensate during nonstress periods (e.g., during the sleep period). Because mounting a fight-or-flight response is costly energetically, the heart rate changes at night might be an attempt to balance the daily energy budget and compensate for the energy lost when responding to the chronic stress.
See also: Conservation and Anti-Predator Behavior; Defense Against Predation; Ecology of Fear; Stress, Health and Social Behavior; Trade-Offs in Anti-Predator Behavior; Vigilance and Models of Behavior.
Further Reading Bohus B and Koolhaas JM (1993) Stress and the cardiovascular system: Central and peripheral physiological mechanisms. In: Stanford SC, Salmon P, and Gray JA (eds.) Stress: From Synapse to Syndrome, pp. 75–117. Boston, MA: Academic Press. Cannon WB (1932) The Wisdom of the Body. New York, NY: W.W. Norton. Goldstein DS (1987) Stress-induced activation of the sympathetic nervous-system. Baillieres Clinical Endocrinology and Metabolism 1: 253–278. Reid SG, Bernier NJ, and Perry SF (1998) The adrenergic stress response in fish: Control of catecholamine storage and release. Comparative Biochemistry and Physiology C: Toxicology & Pharmacology 120: 1–27. Stanford SC (1993) Monoamines in response and adaptation to stress. In: Stanford SC, Salmon P, and Gray JA (eds.) Stress: From Synapse to Syndrome, pp. 281–331. Boston, MA: Academic Press. Steen JB, Gabrielsen GW, and Kanwisher JW (1988) Physiological aspects of freezing behavior in willow ptarmigan hens. Acta Physiologica Scandinavica 134: 299–304. Young JB and Landsberg L (2001) Synthesis, storage, and secretion of adrenal medullary hormones: Physiology and pathophysiology. In: McEwen BS and Goodman HM (eds.) Handbook of Physiology; Section 7: The Endocrine System; Volume IV: Coping with the Environment: Neural and Endocrine Mechanisms, pp. 3–19. New York, NY: Oxford University Press.
Introduction When animals are faced with perceived or anticipated dangers from the environment, they initiate a stress response – a generic term for a bewildering suite of physiological and behavioral responses that are designed to help an animal survive these dangers (called stressors because they elicit a stress response). The two best-studied physiological responses are the release of glucocorticoid steroid hormones and the activation of the sympathetic nervous system. Discussion of the glucocorticoid response is presented in other articles and sympathetic activation, usually referred to as the fight-or-flight response, is the subject of this article. The term fight-or-flight dates back to the early twentieth century and is an excellent brief description of the role of sympathetic nervous system activation. Fight-orflight evokes immediacy. Life is hanging in the balance and there is no time for reproduction, mate selection, foraging, digestion, etc. At this precise instant, only survival is important. The fight-or-flight response is the firstline physiological mechanism for giving an animal its best chance for survival. If an animal mounts a fight-or-flight response, it suggests that the animal is reacting quickly, strongly, and immediately in order to survive. The sympathetic nervous system mediates these reactions. Although many stressors can elicit a fight-or-flight response, the stressor most commonly associated with a fight-or-flight response is a predator attack. Predators can have numerous behavioral effects on their prey, including increasing vigilance, decreasing foraging times, changing how animals interact with other individuals (such as flocking or forming herds), and even altering where individual animals choose to live (i.e., changing prey distribution patterns). Predator presence, predator calls, and predator odors can all evoke a fight-or-flight response and even the threat of predation is sufficiently powerful that animals often react as if there were predators present even when there are none. These predator-induced changes in behavior have been studied for decades, but predator pressure can also change hormonal and physiological systems. Predation risk alters the hormonal and physiological regulation of reproduction and appears to have led to the evolution, in some bird species, of the restriction of sleep to one hemisphere of the brain at a time, an adaptation thought to allow the bird to maintain vigilance for predators at all times. The physiological changes associated with predation risk are so powerful that chronic
710
exposure to predator cues is used as a laboratory model for studying human anxiety. Clearly, the fight-or-flight response occupies a critical position in coping with a short-term stressor such as a predator attack. This article presents an overview of how the sympathetic nervous system regulates a fight-or-flight response and how that response might help an animal to survive.
Sympathetic Nervous System The details of sympathetic activation are highly conserved among vertebrates. Although there are some species differences, the broad outlines are present in every species examined, from fish to mammals. This should highlight how central the fight-or-flight response is for survival. Catecholamines The activity of the sympathetic nervous system is primarily regulated by a class of hormones called catecholamines. Epinephrine and norepinephrine are the two primary catecholamines involved in the fight-or-flight response. They are equivalent to adrenaline and noradrenaline, epinephrine/norepinephrine being the names used in the United States and adrenaline/noradrenaline used in Europe. Epinephrine and norepinephrine are produced primarily in neurons (or modified neurons in the case of adrenal tissue). Synthesis begins with the amino acid tyrosine and ends with the rate-limiting conversion to norepinephrine by tyrosine hydroxylase. Epinephrine can then be converted from norepinephrine, using the enzyme phenylethanolamine N-methyltransferase (PNMT). PNMT is then the rate-limiting enzyme for epinephrine production. Both tyrosine hydroxylase and PNMT are often the targets for assays and in situ localizations to determine where, and potentially how much, epinephrine and norepinephrine are being produced. Anatomy The location of epinephrine release depends in part on the species. In mammals, epinephrine is primarily produced in the adrenal medulla – the center portion of the adrenal gland. The adrenal medulla is essentially a modified sympathetic ganglion where each secretory cell
Fight or Flight Responses
is a neuron without an axon. Epinephrine and norepinephrine are released from two different cell populations in the adrenal medulla. Another major source of norepinephrine is nerve terminals of the sympathetic nervous system. Most nonmammalian species, however, lack a well-defined adrenal medulla. In these species, cells that release epinephrine and norepinephrine are embedded in the wall of the kidneys. These cells are called chromaffin and are homologous to cells in the adrenal medulla of mammals. The physiological responses in mammals and nonmammals, however, appear to be essentially identical. When a stressor begins, epinephrine and norepinephrine are released from the adrenal medulla and norepinephrine is released from the sympathetic nerve terminals. Because the secretory cells are neurons, catecholamine release is very quick and effects can be seen in less than a second. Catecholamines orchestrate the entire fight-or-flight response. The amount released, however, is very important. Sympathetic activation is not an all-or-nothing response and the strength of the response can be modulated to the needs of the moment. If too little response is released, the impact on target tissues will be insufficient; too much release, however, is often fatal. Consequently, the amount of epinephrine and norepinephrine released is usually carefully titrated to correspond to the severity of the stressor. Physiological Effects Once released, the catecholamines exert a number of effects throughout the body. Catecholamine-induced changes in the cardiovascular system have been known for almost a century. Catecholamines alter the delivery of nutrients, especially glucose and oxygen, to the brain, heart, lungs, and skeletal muscles, at the cost of the peripheral tissues. They do this by increasing cardiac output, increasing blood pressure, vasodilating arteries in skeletal muscle, vasoconstricting arteries in the kidney, gut, and skin, vasoconstricting veins in general, stimulating the lungs to dilate air passages, and initiating hyperventilation. Although it might seem counterintuitive that catecholamines would exert such opposite effects as both vasodilation and vasoconstriction, the explanation resides in a difference in receptors. Catecholamine receptors come in both a- and b-varieties, both of which have two subforms (a1 and a2, b1 and b2). The a-receptors have higher affinity for norepinephrine, whereas the b-receptors have a higher affinity for ephinephrine. Furthermore, each receptor type mediates different functions. For example, in arteries a1-receptors mediate vasoconstriction, whereas b2-receptors mediate vasodilation. However, the binding dynamics of a- and b-receptors described earlier apply to mammals. Birds have different
711
binding dynamics (both epinephrine and norepinephine bind preferentially to b-receptors) and other taxa may show slight differences as well. Consequently, the physiology of catecholamine function can be richly varied in different species. A second major effect of catecholamines is to increase the energy available to the muscles and brain, especially when glucose is being rapidly consumed during a fight or when fleeing. Catecholamines accomplish this by stimulating the liver to increase the production of glucose, specifically via glycogen breakdown, which is then released for delivery to peripheral tissues. The end result is a quick burst of glucose that can be used by muscles, the brain, and other essential tissues. Catecholamines also stimulate white adipose tissue to release free fatty acids that the liver can then use to produce more glucose. Once extra glucose becomes available in the blood stream, the final step in this process is to get the glucose into the cells that need it. Catecholamines also stimulate increased glucose uptake in these cells. A third major effect of catecholamines is to regulate a number of effects in the skin. Catecholamines vasoconstrict blood vessels in the skin in order to shunt blood preferentially to internal organs, stimulate sweat production, and induce piloerection, the standing up of hairs in their follicles. Piloerection may serve two purposes: to enhance heat retention and to make the animal appear larger and fiercer to rivals and predators. Catecholamines may also regulate facultative changes in skin color in some species, especially to hide from predators. Finally, the nervous system is also a major target for catecholamines. Their major effects in the brain are to increase attention and alertness. This leads to increased performance on cognitive tasks as well as a decrease in muscular and psychological fatigue. Catecholamines also cause the pupils to dilate, which aids in distance vision.
Increases in Heart Rate Measuring the strength of the fight-or-flight response or even determining whether a fight-or-flight response is initiated, is often difficult. One problem is how fast the sympathetic nervous system is activated. Catecholamines are released into the blood so quickly that it is virtually instantaneous. Currently, one of the few techniques available is to measure changes in heart rate as an index of catecholamine release. Basic regulation of cardiac function is common across the vertebrates with epinephrine as the primary mediator of heart rate during exposure to a stressor. Epinephrine is released either directly from nerve terminals or indirectly from the adrenal and binds to b-receptors on the heart. Epinephrine results in an increase in heart rate (tachycardia) after most stressors. Furthermore, the degree of tachycardia depends upon the
712
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strength of the stressor – stronger stressors evoke higher increases in heart rate. The diversity of stressors that can elicit tachycardia is impressive. Much of the work has been done under laboratory conditions, where stressors such as sounds, lighting conditions, novel odors, confinement, and abnormal social groups can stimulate increases in heart rate. In addition, a small but growing number of studies indicate that wild free-living animals increase heart rate in response to stressors such as human disturbance, social interactions, and capture and handling. Social interactions are potent stressors that can result in robust tachycardia. However, animals can modulate these responses. For example, animals can habituate to intermittent social stressors, resulting over time in lower responses to equivalent social situations. Only the animal that wins the social encounter habituates, however. The loser retains, and even augments, its original tachycardia during subsequent encounters. In addition, the degree of tachycardia in the loser can depend upon the individual coping style of the animal. Animals have been shown to have either reactive or proactive coping styles when faced with novel situations. When faced with many, but not all, stressors, animals with reactive coping styles show a stronger activation of the sympathetic nervous system and thus a stronger tachycardia. Although stressors induce tachycardia, the relationship can be reversed experimentally. The degree of tachycardia can be used to infer the strength of a stressor. If a stimulus evokes tachycardia, it is assumed to be a stressor, and if stressor evokes greater tachycardia than another stressor, then the stressor associated with the greater tachycardia is assumed to be the stronger stressor. There are several examples of this type of work. First, increased crowding evokes greater tachycardia, with the subsequent inference that crowding is stressful to these species. Second, increases in heart rate have also been used to show that many species can distinguish between familiar and unfamiliar conspecific calls, suggesting that vocalizations from neighbors are less stressful than vocalizations from strangers. Finally, animals can have robust increases in heart rate by simply watching agonistic interactions by other animals, even though they are not directly involved. This bystander effect suggests that social interactions, even those in which the individual is not directly involved, can elicit far more robust responses than other potentially dangerous stimuli. In fact, tachycardia can be a more sensitive index of a fight-or-flight response than behavior. Animals often use behavior in order to avoid a costly physiological response – in other words, to avoid a fight-or-flight response. The result is that behavioral and physiological responses are often uncoupled. For example, an animal moving away from a disturbance will not necessarily be in the midst of a fight-or-flight response. In fact, it may be moving away
specifically to avoid a potential stressor. Conversely, a number of studies have indicated that tachycardia can show a strong increase without any overt behavioral changes. Birds sitting in a nest, for example, may be acutely aware of a nearby predator, and show marked tachycardia, even though there is no outward change in behavior. Consequently, increases in heart rate are often better indicators of an underlying physiological fight-orflight response than overt changes in behavior. Heart rate can also be used to determine whether freeliving wild animals are affected by putative anthropogenic stressors. Many things that humans do, such as building roads, ecotourism, wilderness sports, etc., are presumed to serve as potent stressors to wildlife. However, this assumption is rarely tested. Even if these activities change a species’ settlement patterns or reproductive success, it is not necessarily true that the activities will induce a physiological fight-or-flight response. Implanted or attached heart rate transmitters, devices that collect heart rate data from freely behaving animals and transmit those data to a remote detection device, can be used to determine whether anthropogenic activities are, in fact, stressors. The evidence to date suggests that the impact of anthropogenic disturbances is more complex than originally thought. Many anthropogenic disturbances elicit robust fight-or-flight responses and thus can clearly be described as stressors, but other disturbances do not. The presence or absence of a fight-or-flight response may be an excellent diagnostic tool to determine what is, or is not, a stressor. Finally, it should be remembered that an increase in heart rate, driven by the sympathetic nervous system, can extract a heavy price. For many years we have known that humans can go into sudden cardiac arrest and die because of severe emotional trauma. Although it is unknown whether this occurs in wild animals, it could be the mechanism underlying reports of trap death where wild animals spontaneously die for no apparent reason when captured. The fight-or-flight response is clearly necessary to escape from predators, but the increase in heart rate can create its own problems.
Decreases in Heart Rate The uncoupling of tachycardia and behavior points out a weakness of the term fight-or-flight. Not all immediate emergency behaviors can be easily categorized as a fight response or a flight response. Flight generally evokes images of animals running/flying away from a predator. However, moving toward a predator may be a better strategy. Several studies indicate that moving toward an attacking predator, thereby reducing the predator’s maneuvering time, can actually decrease predator success. In fact, often the most effective tactic is to freeze and not
Fight or Flight Responses
move at all: a tactic taken to its extreme in those species that feign death. Furthermore, the type of tactic employed often varies, both between individuals and within the same individual over time. Sometimes the individual flees and sometimes it freezes. These behaviors, freezing or moving towards a predator, are not generally considered to be part of the fight-or-flight response, yet are likely regulated by the same mechanisms. Whether an animal flees or freezes when faced with a predator is not always predictable, but the choices are mutually exclusive with respective pluses and minuses. Fleeing immediately is the better choice when there is sufficient distance and speed to outrun the predator. The downside is that the animal also draws the predator’s attention immediately and almost guarantees a chase. Freezing, on the other hand, may allow the animal to elude detection. This response is especially useful if the animal is not yet detected or has an asset, such as nearby young, that needs to stay hidden. The downside of this choice is that it can allow a predator to get lethally close. The decision whether to freeze or flee is complex, partially dependent upon the individual animal’s predilection, its distance to a refuge, and the potential benefit of confusing a predator by being unpredictable. When an animal chooses to freeze, however, there is a very different change in the sympathetic nervous system. In general, the response is bradycardia, not tachycardia. A classic example is the feigned death of species like the opossum. When faced with a predator, the animal will become limp and nonresponsive to poking and prodding. This behavioral response is accompanied by a marked bradycardia. Heart rate plummets regardless of the behavior of the predator. Bradycardia makes sense in this context – if the goal is to appear dead, then decreasing heart rate helps to damp any behavioral and/or physiological responses. Once the danger has passed, however, the classic sympathetic response resumes and a strong tachycardia ensues. Interestingly, freezing behavior is rarely, if ever, seen in captive animals. Sympathetic activation, with its associated tachycardia, appears to be the default response. Freezing, with its attendant bradycardia, appears to require a specific context that is absent in caged animals.
Seasonal Differences in the Fight-orFlight Response All animals seasonally adjust behavioral and physiological responses. Cardiovascular function and the underlying fight-or-flight response is no exception. For example, resting heart rate is lower during the winter than during the summer for many species. In general, seasonal changes are linked to a lower energetic demand resulting from a lower winter metabolism. However, there are also seasonal differences in sympathetic activation in response to a
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stressor. The fight-or-flight response can be modulated depending upon the life-history stage. For example, animals can show a stronger fight-or-flight response to conspecific crowding when they are defending territories in the spring than when they are gregarious in the winter. The fight- or flight response can also be modulated depending upon the physiological state of the animal. When an animal is in a particularly energy-intensive period, such as molt or pregnancy, the fight- or flight response can be dramatically suppressed. The lack of response highlights that the magnitude, and perhaps even the presence, of a fight-or-flight response may depend upon the season and/ or physiological state of the animal. Seasonal and life-history-stage differences in the fight-orflight response are not well studied. However, understanding how and when sympathetic responses are modulated should provide important insights into the survival benefits of the generalized fight-or-flight response. The modulation of sympathetic activation may be related to seasonal changes in the prevalence and severity of stressors. The end result would be an animal fine-tuning its fight-or-flight response in order to maximize effectiveness.
Sympathetic Responses During Chronic Stress The fight-or-flight response seems well-suited to help an animal cope with short-term emergency situations. If a stressor continues for a long time, however, or if a series of short-term stressors continues in rapid succession, many of the short-term emergency responses can themselves become damaging. When this occurs, it is called chronic stress. The constant and/or repeated initiation of the fight-or-flight response can lead to profound disruption of the sympathetic nervous system. For example, chronic stress can lead to coronary heart disease in both humans and animals. Many studies indicate that, over time, chronic stress leads to a lowering of the magnitude of heart rate elevations in response to a variety of stressors. In other words, chronic stress leads to a damping of the fight-or-flight response. The chronically stressed animal can no longer mount a robust sympathetic response to a novel stressor. This decrease is often interpreted as habituation to the stressor, but other data suggest that this might be too simple an explanation. Stores of both epinephrine and norepinephrine are depleted during chronic stress, which results in diminished release of both hormones. This appears to be the underlying mechanism that results in the attenuated fight-or-flight response. If the fight-or-flight response is indeed down-regulated during chronic stress, it would have tremendous fitness implications. An appropriate fight-or-flight response, necessary to survive stressors in the wild, would be compromised. This suggests that chronic stress greatly impacts on
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an animal’s potential survival, especially in terms of evading predators. In contrast, other studies show long-term increases in heart rate during chronic stress. The increase is in both basal heart rates, indicating chronic sympathetic overstimulation, and in the heart rate response to a stressor, that is the fight-or-flight response. The underlying mechanism appears to be increased synthesis and storage of catecholamines, which may allow the animal to respond stronger to a novel stressor. Note that the two sets of studies come to completely opposite results. One set shows a decrease in catecholamines, leading to decreases in the fight-or-flight response, and the other set shows an increase in catecholamines, leading to increases in the fight-or-flight response. The reasons for this disparity are currently unknown, but a difference in individual coping styles is one candidate. The impact of heart rate changes during chronic stress could also be ameliorated over the course of the day. In some models of chronic stress, the heart rates recover quickly once the chronic stress ends. This suggests that the chronic stress-induced changes are not long-lasting. Furthermore, most chronic stress models apply stressors only during a portion of the 24 h cycle (e.g., during the active period). The heart rate can often recover and even overcompensate during nonstress periods (e.g., during the sleep period). Because mounting a fight-or-flight response is costly energetically, the heart rate changes at night might be an attempt to balance the daily energy budget and compensate for the energy lost when responding to the chronic stress.
See also: Conservation and Anti-Predator Behavior; Defense Against Predation; Ecology of Fear; Stress, Health and Social Behavior; Trade-Offs in Anti-Predator Behavior; Vigilance and Models of Behavior.
Further Reading Bohus B and Koolhaas JM (1993) Stress and the cardiovascular system: Central and peripheral physiological mechanisms. In: Stanford SC, Salmon P, and Gray JA (eds.) Stress: From Synapse to Syndrome, pp. 75–117. Boston, MA: Academic Press. Cannon WB (1932) The Wisdom of the Body. New York, NY: W.W. Norton. Goldstein DS (1987) Stress-induced activation of the sympathetic nervous-system. Baillieres Clinical Endocrinology and Metabolism 1: 253–278. Reid SG, Bernier NJ, and Perry SF (1998) The adrenergic stress response in fish: Control of catecholamine storage and release. Comparative Biochemistry and Physiology C: Toxicology & Pharmacology 120: 1–27. Stanford SC (1993) Monoamines in response and adaptation to stress. In: Stanford SC, Salmon P, and Gray JA (eds.) Stress: From Synapse to Syndrome, pp. 281–331. Boston, MA: Academic Press. Steen JB, Gabrielsen GW, and Kanwisher JW (1988) Physiological aspects of freezing behavior in willow ptarmigan hens. Acta Physiologica Scandinavica 134: 299–304. Young JB and Landsberg L (2001) Synthesis, storage, and secretion of adrenal medullary hormones: Physiology and pathophysiology. In: McEwen BS and Goodman HM (eds.) Handbook of Physiology; Section 7: The Endocrine System; Volume IV: Coping with the Environment: Neural and Endocrine Mechanisms, pp. 3–19. New York, NY: Oxford University Press.