Ecological Bases of Hormone-Behavior

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” responsethe 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 u

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