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AMER. ZOOL., 38:191-206 (1998)
Ecological Bases of Hormone-Behavior Interactions: The "Emergency Life History Stage"1
JOHN C. WINGFIELD,2 DONNA L. MANEY, CREAGH W. BREUNER, JERRY D. JACOBS, SHARON LYNN, MARILYN RAMENOFSKY, AND RALPH D. RICHARDSON*
Department of Zoology, University of Washington, Seattle, Washington 98195 •Department of Psychology, University of Washington, Seattle, Washington 98195
SYNOPSIS. Superimposed upon seasonal changes in morphology, physiology and behavior, are facultative responses to unpredictable events known as labile (i.e., short-lived) perturbation factors (LPFs). These responses include behavioral and physiological changes that enhance survival and collectively make up the "emer- gency" life history stage. There is considerable evidence that glucocorticosteroids, and other hormones in the hypothalamo-pituitary-adrenal (HPA) cascade, initiate and orchestrate the emergency life history stage within minutes to hours. This stage has a number of sub-stages that promote survival and avoid potential deleterious effects of stress that may result from chronically elevated levels of circulating glucocorticosteroids over days and weeks. These sub-stages may include: redirec- tion of behavior from a normal life history stage to increased foraging, irruptive- type migration during the day, enhanced restfulness at night, and elevated gluco- neogenesis. Once the perturbation passes, glucocorticosteroids may also promote recovery. Additional evidence from birds indicates that glucocorticosteroid re- sponses to a standardized capture, handling and restraint protocol are modulated both on seasonal and individual levels. Field work reveals that these changes in responsiveness to LPFs have ecological bases, such as reproductive state, body condition etc., that in turn indicate different hormonal control mechanisms in the HPA cascade.
INTRODUCTION
Most of us interpret "emergency" re- sponses of animals as the "fight-or-flight" response—the massive release of catecho- lamines by adrenal medullary cells (chro- maffin) that increase heart rate, mobilize glucose, etc., within seconds (e.g., Axelrod and Reisine, 1984; Sapolsky, 1987; Johnson et al., 1992). This response is triggered by sudden threatening environmental events such as attack by a predator or dominant conspecific, and it serves to facilitate im- mediate and extreme physical exertion to escape. The fight-or-flight response is usu- ally over within seconds (assuming suc- cessful escape) and the individual returns to normal activity within minutes. Over the past twenty years accumulating evidence
1 From the Symposium Animal Behavior: Integra- tion of Ultimate and Proximate Causation presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 26-30 December 1996, at Al- buquerque, New Mexico.
2 E-mail: [email protected]
suggests another "emergency" response may exist that involves interruption of the life history cycle and re-direction of behav- ior and physiology towards survival. It is distinct from the "fight-or-flight" response in that it takes several minutes or even hours to develop and results in a more long- lived (hours or days, even weeks) interrup- tion of normal activities such as breeding. This "new" phenomenon also raises ques- tions about proximate and ultimate causa- tions. Why has the emergency response evolved and how is it orchestrated?
Organisms have a characteristic series of life history stages that makes up their life cycle (Jacobs, 1996). A highly simplified series of life history stages in birds is pre- sented in Figure 1. The winter (non-breed- ing) stage and breeding stage each have unique sets of sub-stages. Transition from stage to stage is regulated by hormone se- cretions, as is the activation of sub-stages within a stage. Progression of stages and timing are determined by predictable
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192 J. C . WlNGFIELD ETAL.
Winter (non- breeding stage)
Breeding stage
TABLE 1. Labile perturbation factors.
Body condition Social status Territory or home range
Gonadal maturation courtship,
territorial behavior ovulation
parental phase
Transitory emergency stage
Facultative bohBvioml snd physiological
FIG. 1. A highly simplified series of life history stages in birds. The winter (non-breeding) stage and breeding stage have unique sets of sub-stages. Transi- tion from stage to the next is regulated by hormone secretions as is the activation of sub stages within a stage. Progression from stage to stage and timing of a specific stage are determined by predictable changes in the environment (e.g., photoperiod). However, the emergency life history stage may be triggered at any time by unpredictable events in the environment (see labile perturbation factors in Table 1). This transitory emergency stage has its own unique set of sub stages. After the perturbation passes, the individual can return to the original life history stage. If the perturbation was long lived then the next, or an appropriate life history stage for that time of year will be assumed. Modified from Jacobs (1996) and Wingfield et al. (1997).
changes in the environment {e.g., photope- riod). However, the emergency life history stage may be triggered at any time by un- predictable events in the environment (Ja- cobs, 1996; Wingfield et al., 1997). This transitory emergency stage has its own unique set of sub-stages. After the pertur- bation passes, the individual can return to the original life history stage. If the pertur- bation is long lived then the next, or an ap- propriate, life history stage for that time of year will be assumed.
The unpredictable environmental factors that trigger an emergency life history stage have been termed "labile perturbation fac- tors" (LPFs, Jacobs, 1996). It is important to understand that these factors are unpre- dictable (can occur at any time of year), and they are usually transitory (i.e., labile), al- though in recent years human disturbance and pollution may result in "permanent perturbations." There are two major types of LPFs-direct and indirect (Table 1, see
Loss of eggs or young to predator
Loss of eggs or young to short se- vere storm
Brief disturbance (e.g., human)
Direct
Prolonged severe weather Interspecific competition Loss of mate Pollution Habitat change or loss Prolonged disturbance (e.g.,
human)
Expanded from, Wingfield (1988, 1994).
Wingfield, 1988, 1994; Jacobs, 1996). In- direct LPFs result in loss of a nest and young, or temporary deterioration of the habitat. The individuals involved may not trigger an emergency life history stage, but may initiate a fight or flight response. Such unpredictable disturbances are over quickly and the individual continues in its life his- tory stage appropriate for that time of year. Increased glucocorticosteroids may be, but usually are not, involved (Wingfield, 1988). Direct LPFs, on the other hand, affect the individual directly by decreasing available food resources, increasing energetic de- mands (e.g., especially bad weather), or re- stricting access to resources by disturbing optimal habitat (see Wingfield, 1988). In- creased interspecific competition may also result in restricted access to resources, fol- lowed by adjustment of home range and habitat partitioning (Repasky and Schluter, 1994), or at least an increase in energy re- quired to compete for those resources. In these cases, the emergency life history stage is triggered. Although in this paper we will focus primarily on birds, the emer- gency life history stage concept may be widely applicable to all vertebrates—at least at the level of behavioral responses to unpredictable events (e.g., Clutton Brock, 1991).
THE EMERGENCY LIFE HISTORY STAGE
There are several clearly definable events that make up the emergency life history stage in response to LPFs. These have been summarized by Wingfield and Ramenofsky (1997) and are expanded here under four major headings:
1. Deactivation of territorial behavior/dis- integration of social hierarchies:
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THE EMERGENCY LIFE HISTORY STAGE 193
a) Reproduction and associated behavior, seasonal migration or wintering strategies are suppressed.
b) Social relationships may be suspended temporarily.
2. Activation of emergency behavior: a) Seek or remain in a refuge. If food
supply is not compromised, then the best strategy may be to find shelter and "ride- out" the LPF.
b) Move away from the source of per- turbation. If food resources are compro- mised in any way such that negative energy balance is likely, then the best strategy would be to leave and seek alternate habi- tat.
c) Seek a refuge and try to ride out the LPF at first, but then leave if conditions do not improve. The time spent in a refuge be- fore leaving may be a direct function of stored energy reserves. Note that the indi- vidual should leave while energy stores are still sufficient to fuel a flight.
3. Mobilization of stored energy reserves: Since in 2b and c, negative energy bal-
ance is likely, then stores of fat should be tapped. In many cases gluconeogenesis may include mobilization of proteins as well.
4. Settlement in alternate habitat or return to the original site—termination of the emergency life history stage:
a) If the individual remains in its original habitat, then the normal life history stage can be assumed immediately after the LPF has abated.
b) If the individual leaves, then suitable habitat should be identified and the individ- ual can then settle and resume the normal series of life history stages.
c) In many cases, the individual may re- turn to its original habitat once the LPF has passed.
d) Recovery following an emergency life history stage may be a critical component of the whole process.
Evidence to date suggests that the behav- ioral and physiological components of the emergency life history stage are similar, if not identical, at all times of year, and re- gardless of the life history stage from which it may have been triggered (Jacobs, 1996).
It is then logical to propose that the mech- anisms by which this stage is initiated, maintained and terminated may be the same at all times of year and throughout the life cycle of the individual. We propose that neuropeptides associated with the hypoth- alamo-pituitary-adrenal cortex (HPA) axis, adrenocorticotropin (ACTH) and glucocor- ticosteroids regulate the emergency life his- tory stage (e.g., Wingfield, 1994), although it is certain that other endocrine secretions may also be involved. Many hormones have been identified in classical responses to stress in vertebrates, and since many as- pects of the emergency life history stage are superficially similar to stress, it is tempting to draw parallels. However, evidence is ac- cumulating that the emergency life history stage is a mechanism by which individuals avoid stress thus enhancing survival and potentially lifetime reproductive success (Wingfield et al, 1997).
The hypothalamo-pituitary-adrenal axis It has been known for decades that a host
of obnoxious agents (stressors) activate the hypothalamo-pituitary-adrenal axis result- ing in marked elevation of glucocorticoste- roid secretion. Although they orchestrate many of the physiological, morphological and behavioral responses to stress, other hormones are also involved (e.g., Axelrod and Reisine, 1984; Munck et al, 1984; Johnson et al, 1992). The actions of glu- cocorticosteroids during this so-called "stress-response" attracted our attention at first because of the apparent parallels of the emergency life history stage and a classical stress response. Owing to constraints of space we will focus primarily on the actions of opioids and glucocorticosteroids (Table 2). Because the measurement of plasma (3- endorphin levels has proved technically dif- ficult, there are few studies addressing its action in free-living individuals. However, it is known to influence reproductive be- havior, analgesia, and feeding behavior, making this peptide an ideal candidate for involvement in the emergency life history stage. We also include the peptide ACTH because it is released during the initiation of the emergency life history stage, is co- released with p-endorphin (Guillemin et al.,
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194 J. C . WlNGRELD ETAL.
TABLE 2. Effect of Corticosterone in an Emergency Life History Stage.
Rapid {i.e., short term.
minutes to hours)
Suppress reproductive be- havior
Regulate immune system Increase gluconeogenesis Increase foraging behav-
ior Promote escape (irruptive)
behavior during day Promote night restfulness
by lowering standard metabolic rate
Promote recovery on re- turn to normal life his- tory stage
Chronic (i.e.. long term. days to weeks)
Inhibit reproductive sys- tem
Suppress immune system Promote severe protein
loss Disrupt second messenger
systems Neuronal cell death Suppress growth and
metamorphosis
Modified and expanded from Wingfield (1994).
1977), and binds to opioid receptors (Ter- enius, 1977).
Wingfield (1994) suggested that there may be two distinct types of response to glucocorticosteroids during a stress re- sponse. By far the most well studied are chronic effects induced by many days or even weeks of exposure to continual high circulating levels of glucocorticosteroids re- sulting from prolonged exposure to stress. These effects (Table 2) include total failure of reproductive function, increased suscep- tibility to disease owing to suppression of the immune system, neuronal cell death (particularly in the hippocampus), severe protein loss (for gluconeogenesis), disrup- tion of the arachidonic acid cascade, and inhibition of growth and metamorphosis (e.g., Axelrod and Reisine, 1984; Munck et al, 1984; Johnson et al., 1992; Sapolsky 1987, 1996). Although these effects have immense importance for medicine and ag- riculture, it is difficult to imagine how any one of these states would be adaptive for an organism in the field. Indeed death would be imminent in any of these states. Thus it is unlikely that chronic effects of high circulating levels of glucocorticoste- roids have much biological significance since survival by this time would be virtu- ally zero (Wingfield et al., 1997). It is well documented that severe environmental per- turbations occasionally result in massive mortality in natural populations (see Wing-
field et al., 1997), but presumably there would be strong selection for mechanisms by which such deleterious states are avoid- ed in survivors. Therefore, the short term effects of elevated glucocorticosteroids (over minutes to hours) may be highly adaptive in avoiding the severe stressed state. These short term effects are also sum- marized in Table 2. It is these effects that may orchestrate the emergency life history stage and avoid the clearly severe, and very likely fatal, consequences of chronic high levels of glucocorticosteroids and other hor- mones of the HPA axis. The evidence for short term effects of HPA hormones con- sistent with the emergency life history stage are as follows.
Suppression of reproductive behavior One of the hallmarks of an emergency
life history stage is that individuals redirect their activities from those typical of the nor- mal life history stage, to others more con- ducive to survival. There are many ac- counts of abandonment of breeding terri- tories and offspring in response to LPF-like environmental events (e.g., Gessamen and Worthen, 1982; Clutton Brock, 1991), sug- gesting that redirection of behavior may be widespread. At first this may appear mal- adaptive because reproductive success be- comes zero. However, temporary suspen- sion of breeding activity may actually en- hance lifetime reproductive success by al- lowing an individual to survive the perturbation in good condition so that it can then breed again at the earliest opportunity.
Glucocorticosteroids.—In free-living pied flycatchers, Ficedula hypoleuca, im- plants of corticosterone reduced parental behavior in both sexes (Silverin, 1986). Nestlings were fed less, fewer fledglings re- sulted, and young that did fledge weighed less than fledglings from control implanted birds. Another group that received implants designed to give even higher circulating levels of corticosterone resulted in complete abandonment of nests with zero reproduc- tive success (Silverin, 1986). In breeding male song sparrows, Melospiza melodia, similar implants of corticosterone resulted in marked reduction of territorial aggres- sion. Furthermore, plasma levels of testos-
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THE EMERGENCY LIFE HISTORY STAGE 195
terone were still in the range typical of this period in the reproductive cycle, suggesting that corticosterone may override the effects of testosterone in activation of territorial ag- gression (Wingfield and Silverin, 1986). Similarly in side-blotched lizards, Uta stansburiana, implants of corticosterone significantly reduced home range size and activity if control implanted lizards were also present (DeNardo and Sinervo, 1994a). However, if all individuals at a site were implanted with corticosterone, there was no decrease in home range size or activity, suggesting that corticosterone may reduce the effectiveness of males in retaining their home ranges when in competition with nor- mal males. In another experiment, it was shown that if lizards were also implanted with testosterone, then corticosterone treat- ment still resulted in reduced home ranges if control males were present (DeNardo and Sinervo, 1994fc). These data suggest further that the effects of corticosterone override any effect of testosterone on spatial behav- ior. The mechanisms underlying these be- havioral responses remain unknown. Glu- cocorticosteroids also may directly suppress reproductive behavior. Subcutaneous injec- tion of corticosterone profoundly inhibits courtship behavior in male rough-skinned newts, Taricha granulosa (Moore and Mil- ler, 1984).
$-endorphin.—The effects of opioids on reproductive behavior are well known and too extensive to cover in detail here. Ex- periments with antagonists and agonists have demonstrated an inhibitory role for both central and circulating opioids. In the rough-skinned newt, stress-induced inhibi- tion of courtship can be reversed by treat- ment with naloxone, an opioid antagonist (Miller and Moore, 1982). In rats, central infusion of P-endorphin causes a decrease in mounting by males and an inhibition of lordosis in females (Meyerson and Berg, 1977; Sirinathsinghji, 1984). Intraventricu- lar infusion of corticotropin-releasing factor (CRF) results in suppression of lordosis that is reversible by (B-endorphin antagonists (Sirinathsinghji et al., 1983a, b). In female white-crowned sparrows, Zonotrichia leu- cophrys gambelii, central infusion of P-en- dorphin strongly inhibits copulation solici-
tation whereas naloxone enhances it (Ma- ney and Wingfield 1998). The mechanism of opioid-induced suppression of reproduc- tive behavior is unknown, but there is evi- dence that p-endorphin acts within the brain to suppress gonadotropin-releasing hor- mone (GnRH) neuronal systems (see Siri- nathsinghji, 1984; Fan and Ottinger, 1996).
Promotion of gluconeogenesis Glucocorticosteroids play a key role in
promoting gluconeogenesis, especially from protein, in many vertebrate taxa (Chester-Jones et al., 1972). In mammals, glucocorticosteroids play a central role in metabolic responses to stress by sustaining gluconeogenesis by increasing the supply of hepatic gluconeogenic precursors and by maintaining glycogen availability in the liv- er (e.g., Fujiwara et al., 1996). Acute in- creases in glucocorticosteroids increase the gluconeogenic conversion of alanine to glu- cose by elevating uptake of alanine by the liver, and may also be accompanied by a transient decrease in insulin to further en- hance gluconeogenesis (Goldstein et al., 1992). Similar mechanisms may operate in birds, although increased glucose (or gly- cogen) may not be the only result. In song sparrows and pied flycatchers, corticoste- rone treatment results in apparent loss of protein from flight muscles, but no change in body weight because fat depots increased markedly (Wingfield and Silverin, 1986; Silverin, 1986). Similar effects were found in captive dark-eyed juncos, Junco hyemal- is, (Gray et al, 1990). Furthermore, al- though adipose lipoprotein-lipase (LPL) ac- tivity was unchanged, the concentration of LPL in muscle increased significantly even though muscle mass declined. These data are consistent with the hypothesis that fly- ing birds utilize fatty acids as a major fuel for flight rather than glycogen.
Ward (1969) and others have suggested that the pectoralis flight muscles of birds may be important reservoirs of readily- mobilizable protein for reproduction and possibly flight. A morphological study by Kendall et al. (1973) of flight muscles of Quelea quelea, suggested that soluble pro- teins may be stored in mitochondria and be- tween myofibrillar bundles in sarcoplasm.
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196 J. C . WlNGFIELD ETAL.
However, such stores, if they exist, are dif- ficult to quantify morphologically. Honey (1990) devised a biochemical method to separate soluble and structural (contractile) proteins in avian muscle by extraction in low or high salt phosphate buffers. When corticosterone was implanted into captive house sparrows, Passer domesticus, there was a significant decline in body weight and particularly in weight of pectoralis muscles compared with controls. Further, this loss of mass in muscle was due to a significant decline in soluble protein frac- tions. Structural (myofibrillar) fractions did not differ between treatments. The influenc- es of corticosterone, and other hormones, on gluconeogenesis and utilization of pro- tein require further study on wild birds in different life history stages.
Regulation of the immune system It is now well known that unpredictable
events in the environment can stimulate re- lease of cytokines and monokines. These hormones of the immune system can inter- act extensively with other components of the endocrine system and in turn can mod- ify behavior {e.g., Munck et al., 1984; Cun- ningham and De Souza, 1993). Although our knowledge of these effects in non- mammalian vertebrates is sparse, it has been demonstrated that when male Western fence lizards, Sceloporus occidentalis, are injected with human interleukin-1 fi (IL-1), they show decreased activity (especially in the morning hours) compared to saline in- jected controls and untreated animals. This suppression of activity is similar to that seen in lizards infected with malaria (Dun- lap and Church, 1996). The authors suggest that IL-1 may mediate pathogen-induced changes in activity. Whether these hor- mones may also mediate other aspects of activity in an emergency life history stage in general awaits further study.
Increase in foraging behavior Glucocorticosteroids.—As in mammals,
there is evidence that glucocorticosteroids, along with other metabolic hormones, are important in the regulation of food intake {e.g., Richardson et al., 1995). Implants of metyrapone (a blocker of 11 |3-hydroxylase,
an enzyme essential for the synthesis of glucocorticosteroids) decreased foraging behavior (a combination of searching, scratching, pecking, and actual food intake) in male white-crowned sparrows and re- placement therapy with implants of corti- costerone increased foraging (Wingfield et al., 1990). However, implants of corticoste- rone into otherwise untreated white- crowned sparrows and song sparrows tend- ed to increase foraging (Astheimer et al., 1992), but this was not significant, and had no effect in dark-eyed j uncos (Gray et al., 1990). It is possible that corticosterone may play a "permissive" role in the regulation of food intake. Other factors acting central- ly may also be important, as has been shown in mammals (Leibowitz et al., 1984).
$-endorphin.—Endogenous opioids are well-known to affect feeding behavior, and may initiate an increase in foraging during the emergency life history stage. Intracere- broventricular beta-endorphin has been shown to increase food intake or feeding behavior in a variety of vertebrates, includ- ing rats (McKay et al., 1981), pigeons (Deviche and Schepers, 1984), and white- crowned sparrows (Maney and Wingfield, 1998). Food deprivation (see Morley et al., 1983) causes beta-endorphin levels to de- crease in the rat hypothalamus, suggesting release of this peptide. Stress-induced feed- ing can be reversed by naloxone, an opioid antagonist (reviewed by Morley et al., 1983). Intramuscular injection of naloxone methobromide, an antagonist that does not cross the blood-brain barrier, decreases feeding in domestic fowl (Denbow and Mc- Cormack, 1990), indicating that endoge- nous opioids may also modulate feeding be- havior at sites outside the CNS.
Promotion of diurnal escape (irruptivel shelter) behavior
Corticosterone treatment of captive male white-crowned sparrows resulted in a de- cline of perch hopping activity over the day (Astheimer et al., 1992), which is consistent with "shelter" behavior related to "riding out" the perturbation factor. This result is particularly compelling since food was available ad libitum and leaving may not
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THE EMERGENCY LIFE HISTORY STAGE 197
confer any advantage. However, if food was removed for 24 hours (to simulate severe storms that often reduce food resources), then corticosterone-treated birds showed a considerable increase in perch hopping ac- tivity exceeding that of controls throughout the day. These data suggest that under con- ditions of reduced food availability, corti- costerone may actually enhance activity, possibly associated with leaving the source of perturbation. Note that this activity is during the day and not at night. In the white-crowned sparrow normal spring and autumn migratory behavior occurs at night (e.g., Wingfield et al, 1990), suggesting that corticosterone-induced activity is a dif- ferent phenomenon consistent with the emergency life history stage (Jacobs, 1996) and not a normal life history stage (e.g., vernal or autumn migrations). Again, cen- tral effects of hormones may be important in distinguishing whether corticosterone has an effect to decrease or increase activity. This is currently under investigation. Note also that in Western fence lizards, IL-1 de- creased activity (Dunlap and Church, 1996). It is possible that such a mechanism may also operate in white-crowned spar- rows.
Promotion of nocturnal restfulness It was originally suggested that since cor-
ticosterone may have marked effects on ac- tivity of birds during an emergency life his- tory stage, then we might predict that this glucocorticosteroid may also increase met- abolic rate. In contrast, implants of corti- costerone actually reduced extended meta- bolic rate in captive white-crowned spar- rows (as measured by oxygen consumption) over night compared with controls (Butte- mer et al, 1991). Control treated birds, as well as birds sampled before treatment, showed episodes of oxygen consumption over a 60 min sampling period at night. Corticosterone treatment did not reduce standard metabolic rate, but eliminated ep- isodes of increased oxygen consumption with a net savings of energy over night. Similar effects were obtained in American goldfinches, Carduelis tristis, pine siskins, C. pinus, and red crossbills, Loxia curvi- rostra (Buttemer et al., 1991). The authors
interpreted these results as enhanced "night restfulness" in an emergency life history stage. Note also that this effect is not con- sistent with nocturnal migratory activity in normal life history stages of vernal and au- tumnal migrations, and further supports the concept of a distinct emergency life history stage with its own suite of hormonal control mechanisms.
Promotion of recovery on return to normal life history stage
Implants of corticosterone into captive song sparrows had little effect on foraging- like behavior when food was removed for 24 hours, but did greatly enhance food in- take when food was returned. Similar, but less marked, effects were seen in male white-crowned sparrows that were treated with corticosterone and had food withheld for 24 hours and then refed (Astheimer et al., 1992). These data suggest an additional role for corticosterone in the recovery phase after a perturbation ceases. Because of its well known role in analgesia, P-endorphin must also be considered here. This aspect of the emergency life history stage deserves further study.
Overview Experimental evidence to date thus sup-
ports the concept of an emergency life history stage that can be triggered by increased cir- culating levels of corticosterone. Although other hormones are undoubtedly involved, it seems clear that the transitory elevation of glucocorticosteroids above normal baseline levels and daily or seasonal changes (levels A and B of Wingfield et al, 1997; Fig. 2) to high concentrations often associated with stress (level C of Wingfield et al, 1997; Fig. 2), results in a suite of physiological and be- havioral responses. These redirect the indi- vidual quickly from "non-essential" activities such as reproduction, territorial behavior, and social hierarchies, to behaviors associated with surviving the perturbation. In this way the individual minimizes the possibility of metabolic debilitation, thus avoiding the det- rimental effects of chronic stress and pro- longed high levels of glucocorticosteroids. Most of the evidence given here comes from birds, but it is highly likely that the concept
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198 J. C. WINGFIELD ET AL.
E c
c o a> to o o
o O
-Level C
- Level B
- Level A ® o ? r o o ) g ) o 3 0 ? S > m ' ' 5 c _ 3 — OS
o 5 o o> O c 2 5;
(A
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FIG. 2. Changes in circulating plasma levels of corticosterone (top panel, solid line) and fat depot (lower panel, solid line) in male Puget Sound white-crowned sparrows (Zonotrichia leucophrys pugetensis) during a normal breeding cycle (i.e., no labile perturbation factors). Note the depiction of stages and sub-stages during the breeding period (X axis). In May 1980 a prolonged rain and wind storm resulted in abandonment of nests and territories. Renesting occurred in June and July after weather conditions became more normal. The cross hatched bars show that cortico- sterone levels (upper panel) were greatly elevated over the year with no storm even though all birds were in the same reproductive sub-stage. Later, when renesting occurred, corticosterone levels had returned to normal. Level A is the absolute baseline of corticosterone, Level B is the limit of normal variation of corticosterone levels in the absence of perturbation factors (i.e., normal daily and seasonal cycles); and Level C is the limit of variation above Levels A and B. Perturbations factors result in transitory increases in corticosterone above Level B (see Wingfield et al., 1997 for details). Fat depot (cross hatched bars, lower panel) in males during the storm were depleted but had returned to normal when renesting. Numbers by points are sample sizes, vertical bars arc standard errors of the means. Top panel from Wingfield et al. 1997; bottom panel redrawn from Wingfield and Farner (1978) and Wingfield et al. (1983).
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THE EMERGENCY LIFE HISTORY STAGE 199
of emergency life history stage is applicable to other vertebrate taxa as well. The next question is, do individuals in the field that are challenged by LPFs actually show elevations in glucocorticosteroids, and how quickly is the emergency life history stage initiated?
TRIGGERING THE EMERGENCY LIFE HISTORY STAGE: THRESHOLDS AND TIME COURSE
Field investigations of bird populations responding to labile perturbation factors
There are now numerous studies indicat- ing that individuals responding to unpre- dictable events in the environment, such as direct LPFs, show elevated levels of corti- costerone in blood consistent with devel- opment of an emergency life history state. This response appears to occur both in breeding and non-breeding life history stages, and may be possible in other stages as well (see Wingfield, 1984, 1988, 1994 for reviews). For example, male white- crowned sparrows that had abandoned their nests and territories in response to a severe and prolonged storm in May 1980 had greatly elevated circulating levels of corti- costerone compared with males sampled in a year with no storm (Fig. 2, top panel; Wingfield and Farner, 1978; Wingfield et al, 1983). Note that in the year with fan- weather, baseline corticosterone levels in- creased in breeding males (within level B of Wingfield et al, 1997) and declined thereafter (level A of Wingfield et al, 1997). Later in the season, after the severe storm had passed and birds were renesting, plasma levels of corticosterone had returned to normal for that time of year (i.e., within level B, Fig. 2). During the storm, subcu- taneous fat depots were virtually depleted, but returned to normal after the storm had passed when renesting was initiated (Fig. 2, bottom panel). Thus corticosterone levels were high when an emergency life history stage had been triggered. It has been sug- gested that the effects of corticosterone on territorial behavior do not occur via sup- pression of sex steroid hormones that nor- mally activate reproductive behavior. In Figure 3 it can be seen that during the storm of 1980, male white-crowned sparrows had normal levels of luteinizing hormone and
testosterone, thus supporting the hypothesis that corticosterone may be acting directly to suppress expression of reproductive behav- ior rather than indirectly through decreased secretion of sex steroids that activate such behavior. Further research is needed to de- termine the mechanisms and locus of cor- ticosterone action in this regard.
These responses are not restricted to the breeding stage. Severe winter weather that triggered emergency life history stages was accompanied by elevated plasma levels of corticosterone in dark-eyed juncos (Rogers et al, 1993); Harris' sparrows, Zonotrichia querula, (Rohwer and Wingfield, 1981); and common diving petrels, Pelecanoides urinatrix, (Smith et al, 1994). It seems likely, then, that not only does the emer- gency life history stage have common char- acteristics regardless of the normal life his- tory stage during which it may be triggered, but also that it is dependent upon a rise of glucocorticosteroids and other hormones of the HPA axis.
Time courses Another question that needs to be re-
solved is how quickly a LPF can trigger an emergency life history stage. This will, of course, depend to a great extent on the se- verity and intensity of the LPF. Experimen- tal evidence suggests that in white-crowned sparrows food withdrawal results in a de- crease in blood glucose and an increase in free fatty acid levels for up to 22 hours of fasting. Plasma levels of corticosterone rose within at least 2 hours of fasting (Richard- son, 1996). More recent evidence suggests that even as little as one hour without food stimulates an increase in corticosterone lev- els and heightened perch hopping activity (S. Lynn and J. C. Wingfield, unpublished). Furthermore, non-invasive administration of corticosterone to male white-crowned sparrows (via feeding of meal worms in- jected with vehicle, or corticosterone) re- sulted in an increase in plasma levels of corticosterone within 5-10 min and height- ened perch hopping activity within 15 min (Breuner et al, 1998). These data clearly suggest that even short term fasting, as would be expected during onset of a severe storm (a form of direct LPF), results in an
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200 J. C . WlNGFIELD ET AL.
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FIG. 3. Changes in circulating plasma levels of luteinizing hormone (LH, top panel, solid line) and testosterone (lower panel, solid line) in male Puget Sound white-crowned sparrows (Zonotrichia leucophrys pugetensis) during a normal breeding cycle (i.e., no labile perturbation factors). Note the depiction of stages and sub-stages during the breeding period (X axis). In May 1980 a prolonged rain and wind storm resulted in abandonment of nests and territories. Renesting occurred in June and July after weather conditions became more normal. The cross hatched bars show that both LH and testosterone levels were not affected by the storm even though nests and territories were abandoned—behavior known to be under control of sex steroids in this species. Numbers by points indicate sample sizes, vertical bars are standard errors of the means. Redrawn from Wingfield and Farner (1978) and Wingfield et al. (1983).
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THE EMERGENCY LIFE HISTORY STAGE 201
increase in circulating glucocorticosteroids within at least an hour, and that behavioral responses consistent with the emergency life history stage follow within minutes. These phenomena are entirely consistent with observations of bird populations in the field as they respond to natural LPFs. Mechanisms of these rapid responses are currently under investigation.
A model to explain biological context for the emergency life history stage at population and individual levels
The evidence is compelling that the emergency life history stage can be trig- gered within minutes to hours at any, or at least most, times of year, and by a whole spectrum of LPFs. However, the question of whether a common physiological pathway exists by which such diverse environmental information is transduced into secretions of the hypothalamo-pituitary-adrenal axis re- mains. Much further work is needed at the central level, but we have postulated the following scheme which may provide a uni- fying framework to explain how physical and social LPFs may trigger an emergency life history stage under extremely diverse conditions. We admit that the model is very simplistic, but we feel it has heuristic value as a beginning to understand the possible common themes underlying these phenom- ena.
The framework is based on a simple en- ergetic theme. Here we propose E to rep- resent the energy required by an individual to survive day to day and pursue its activ- ities as demanded by the progression of normal life history stages. It makes no as- sumptions or adjustments for specialized nutrient requirements, vitamins etc., al- though these could easily be worked into the model if nutritionists required. We then suggest the following:
EG = Energy to be gained from food in environment
EE = Existence energy (i.e., maintenance- level = resting metabolic rate)
El = Energy required to obtain food, pro- cess and assimilate it under ideal conditions
EO = Additional energy required to ob- tain food under non-ideal conditions
In the theoretical example given in Fig. 4, EG, El and EE remain constant over time (such as the annual cycle of seasons). In reality of course, they will vary as a func- tion of predictable changes in the environ- ment. We have kept them constant here for simplicity and illustrative purposes. Nor- mally, EG - (El + EO + EE) > 0 and thus the individual should remain in an appro- priate life history stage. However, if a LPF should occur, (Fig. 4), then the additional energy required to obtain food may increase such that EG - (El + EO + EE) < 0. In this case the individual should trigger an emergency life history stage. Note that once the perturbation passes and EG - (El + EO + EE) > 0 once again, then the individual can return to a life history stage appropriate for that time. On the other hand, if alternate habitat is discovered that allows positive energy balance, then the individual may set- tle there and resume its normal life history stage. The duration of the perturbation fac- tor can vary resulting in short duration of the emergency life history state (Fig. 4, up- per panel) to long duration (Fig. 4, lower panel). In the latter case, the original life history stage may be inappropriate, and the next stage, or most appropriate one may be assumed. In this way the individual is able to adjust life history stages to maximize survival and ultimately lifetime reproduc- tive success in response to both predictable and unpredictable environmental events.
MODULATION OF ADRENOCORTICAL RESPONSES TO LABILE PERTURBATION
FACTORS
There are now several lines of evidence suggesting that in birds, the sensitivity of the hypothalamo-pituitary-adrenal (HPA) axis to LPFs changes at the population level (i.e., among life history stages) and at the individual level (e.g., Wingfield, 1994; Wingfield et al, 1995). Most of these stud- ies have been conducted in the field and use a standardized test to determine the sensi- tivity of the HPA axis. Because different species are acclimated to widely different habitats, and any one population may move
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202 J. C . WlNGFIELD ETAL.
Storm, or other perturbation, increases Eo
Emergency life history
stage triggered
Return to original
life history stage
Emergency Return to life history appropriate
stage life history triggered Tjmg 8 t a 9 e
FIG. 4. Theoretical depiction of when an emergency life history stage should be triggered. Over time (such as annual cycle of seasons), we assume here that E (energy as defined by all nutrients an organism needs to survive and breed), and its components EG = energy to be gained from food in environment; EE = existence energy; and El = energy required to obtain food, process and assimilate it under ideal conditions remain constant. EO = additional energy required to obtain food under non-ideal conditions increases because of a storm or other labile perturbation factor. Then if EG - (El + EO + EE) > 0 the individual should remain in an appropriate life history stage. If EG - (El + EO + EE) < 0 then the individual should trigger an emergency life history stage. Periods of the perturbation may be short (upper panel) or long (lower panel). Note also that EG, El and EE may all change seasonally but in a predictable manner. EO increases as a result of unpredictable perturbation factors.
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THE EMERGENCY LIFE HISTORY STAGE 203
among several habitats during its annual cy- cle of life history stages, it is not possible to use "natural" LPFs such as temperature extremes, food restriction etc. across all species. Thus, we have developed the "cap- ture stress" protocol in which birds are cap- tured, handled and restrained in a cloth bag for periods up to one hour. During this time small blood samples are collected at inter- vals (within 1-2 min of capture and then at 5, 10, 30 and 60 min of handling and re- straint) for measurement of corticosterone. We can then compare the baseline value at capture (indicative of the level in the free- living animal just prior to capture), the rate and degree of increase, and the maximal level of corticosterone attained (e.g., Wing- field, 1994). While we admit that this pro- cedure is not the most perfect way to assess sensitivity of the HPA axis to LPFs, all populations thus far studied react to capture with increased heart rate, respiration rate, and struggle to escape as expected (individ- uals try to avoid what to them is likely a predation attempt). It also is a powerful way to stimulate marked increases in cir- culating glucocorticosteroid levels and al- though this protocol bears little relation to many of the diverse LPFs known, it does allow us to assess sensitivity of the HPA axis as a measure of responsiveness to acute unpredictable stimuli. We can test many in- dividuals and populations in exactly the same way and thus test hypotheses as to why modulation or individual differences exist. With these provisos in mind we can then test hypotheses as to possible ecolog- ical bases of these endocrine phenomena under field conditions that in turn indicate appropriate laboratory experiments to ex- plore mechanisms further.
Modulation at the population level Wingfield (1988) suggested that seasonal
suppression of the HPA axis during the re- productive life history stage may be related to severity of habitat. Although it may be highly adaptive to trigger an emergency life history stage at most times of year, if the breeding season is very short, especially in severe habitats such as the Poles, deserts, high altitudes etc., then it may be advanta- geous to suppress sensitivity of the HPA
axis to LPFs—at least temporarily. Failure to do so may result in frequent interruption of breeding attempts in severe climates. Blunting sensitivity to LPFs would increase costs of breeding and may even increase mortality, but the pay off is increased re- productive success. Evidence for suppres- sion of the sensitivity of the HPA axis to the capture and handling protocol has been obtained for arctic birds (Wingfield et al, 1995) and birds of the Sonoran Desert (Wingfield et al, 1992). Furthermore, this suppression is most marked when in the pa- rental sub stage (Wingfield et al, 1995). Note, however, that this is not a universal property of the HPA axis in birds in ex- treme habitats. Some actually increase sen- sitivity of the HPA axis to LPFs (Astheimer et al, 1995; Wingfield et al, 1995) for rea- sons as yet unknown.
There is also evidence that even if sen- sitivity of the HPA axis to LPFs is sup- pressed, if the LPF is prolonged, then birds have the ability to reactivate adrenocortical responses and trigger an emergency life his- tory stage before individuals become debil- itated. A population of arctic breeding Lap- land longspurs, Calcarius lapponicus, sub- jected to a 3 day storm in mid June, re- mained on their nests for several days but then began to abandon as weather condi- tions failed to improve. Birds captured after abandoning their nests had a rate of in- crease in corticosterone following the cap- ture and handling protocol that was almost an order of magnitude higher than before the storm (Astheimer et al, 1996). These data emphasize the ability for modulation of sensitivity of the HPA axis to LPFs in both directions. Such modulations allow birds to adjust expression of the emergency life history stage very precisely to environ- mental conditions and to their life cycle. Mechanisms underlying these modulations are just beginning to be investigated.
Modulation at the individual level Although there may be marked modula-
tion of sensitivity of the HPA axis to LPFs among populations or within populations from season to season, within these cohorts there may be considerable individual vari- ation. Again, the question "why" comes to
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204 J. C . WlNGFIELD ETAL.
the fore. In white-throated sparrows (Zo- notrichia albicollis), social status and body mass are negatively correlated with inten- sity of the adrenocortical response to cap- ture, handling and restraint. This may ex- plain individual differences at least partially (Schwabl, 1995). We have also found that body condition, particularly the size of fat depots, correlates negatively with sensitiv- ity of the HPA axis to the capture protocol in a number of arctic species (Wingfield, 1994; Wingfield et al, 1995), although this is by no means a universal phenomenon. Individual variation in sensitivity of the HPA axis to LPFs in other species may be have entirely different ecological bases as yet unknown. Endocrine mechanisms un- derlying these modulations also remain to be determined.
CONCLUSIONS
Evidence to date is compelling that an emergency life history stage exists that can be triggered at any, or most, intervals in the life cycle of vertebrates. It is distinct from the "flight-or-flight response because it takes minutes to hours to develop (rather than seconds), and can be triggered by per- turbations of the environment that may not necessarily be immediately life threatening {e.g., bad weather). The hormones in- volved, however, may show considerable overlap between the "flight-or-flight" re- sponse and the emergency life history stage, but the behavioral and physiological effects and mechanisms of action are likely to be different. This emergency life history stage may play a major role in maximizing overall lifetime fitness by redirecting indi- viduals away from non-essential activities (such as reproduction) during environmen- tal perturbations. This would allow survival in the best conditions possible so that when the LPF passes the individual can return to its normal life history stage. If this were reproduction, then renesting would follow. Given the current information available, we can suggest that the behavioral and physi- ological characteristics of the emergency life history stage should be identical, re- gardless of the time of year when it is trig- gered. Also, we suggest that the interactions of hormones in the HPA axis to orchestrate
this stage should be similar at all times of year (but not necessarily among all popu- lations). Further research will now address these issues of action and mechanisms un- derlying the interaction of glucocorticoster- oids and peptides. Of particular interest are the receptors, locations and mechanisms of action at the central level. Most of the work cited here focuses on the class Aves, but we suggest that the emergency life history stage may be triggered in other vertebrates in essentially similar ways. These lines of research also transcend traditional bound- aries of ultimate and proximate mechanisms in biological disciplines by incorporating theoretical modeling, ecology, behavior, physiology, endocrinology and cell and mo- lecular mechanisms.
ACKNOWLEDGMENTS
The authors' work cited here was sup- ported by grants from the Office of Polar Programs, the Division of Integrative Bi- ology and Neurobiology, and International Programs (US/Japan cooperative research grant) from the National Science Founda- tion.
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Corresponding Editor: Paul A. Verrell
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