Hormonal Control of Incubation/Brooding Behavior: Lessons from Wild Birds (pp. 163-169 Proceedings of the WPSA 10th European Poultry Conference, Israel, 1998.) CAROL M. VLECK Department of Zoology and Genetics, Iowa State University, Ames, Iowa 50011, USA More than 90% of all bird species are monogamous within a breeding season. Biparental care of eggs and young is generally the rule for these species, especially for those which do not produce precocial young. Thus the common domesticated species differ from the majority of other birds in the display of parental behavior. The hormonal control of such behavior, however, appears to be similar in all birds, with variations associated with different social systems, phylogenetic histories and ecologies. I have studied the correlation between plasma levels of hormones and behavior in free-living birds of several species and found the following general characteristics. Elevated testosterone appears to be incompatible with assiduous parental care in males. Prolactin is highly correlated with the display of both incubation behavior and brooding/feeding of altricial young. In those species in which non-breeders help raise the young of other birds (cooperative breeders), prolactin levels are elevated in the helpers, sometime even before begging young are present. Many seabirds such as penguins leave the eggs and young for many days to forage at sea while the mate remains at the nest. Despite the absence of tactile stimulation, the foraging birds maintain high levels of prolactin and spontaneously return to the nest to incubate. Vasoactive intestinal peptide is a potent prolactin releasing factor in birds including several species of passerines as well as gallinaceous and columbiform birds, but the interaction of the serotonergic systems may differ among species. Keywords: incubation; parental behavior; prolactin; testosterone; cooperative breeders; incubation patch Introduction Nearly all bird species display parental behavior. The extent of such parental attention to egg and chicks depends upon the developmental maturity of the hatchling which varies along an altricialprecocial spectrum (Starck and Ricklefs, 1998). Birds of the family Megapodiidae (Order: Galliformes) have the most precocial chicks, requiring no post-hatching care, and parents display the most atypical incubation behavior (Frith, 1956). Care of eggs in the megapodes does not involve direct application of heat from a brood patch, but rather often elaborate procedures to maintain temperature using heat sources as such as geothermal, solar, or decomposition of organic material. A few species of birds (particularly the cowbirds and some of the cuckoos) are obligate brood parasites, depositing their eggs in the nests of other species to be incubated and cared for by the host. In essentially all other avian species one or both parents must incubate the eggs until
hatching and then provide some form of post-hatching care. Care of hatchlings ranges from guarding and guiding in most precocial species (as in Anseriformes and Galliformes) to provisioning of all food and intensive brooding for thermoregulation (as in Passeriformes and Psittaciformes). In the majority of species both males and females contribute to care of eggs and young. Since the fitness of an individual is determined directly by its contribution to the genetic pool of the subsequent generation, it is little wonder that natural selection has produced a myriad of behaviors by which parent birds attempt to increase survival of their own offspring. Considering the highly adaptive value of such behavior it is also not surprising that attempts by the poultry industry to reduce the incidence of incubation and brooding behavior have met with limited success (Sharp, 1997). The neural and hormonal basis of parental behavior has been studied extensively in both domesticated and free-living birds of many species, although there is no clear understanding of how the diversity in parental behavior arises from the underlying physiological mechanisms (reviewed in Buntin, 1996). Much of the work on free-living birds has focused on the correlations between plasma levels of the hormone prolactin and parental behavior, and how these vary with social system, ecology and life-history traits. In contrast, much of the work with domesticated species of economic importance has focused on the hypothalamus-pituitary axis and the secretion of prolactin, with the general goal of understanding how broodiness can be inhibited in order to prevent egg production losses that accompany broodiness. Many of these poultry species have been artificially selected for precocial maturation, high egg production, reduced seasonality, and reduced broodiness. In addition, parental behavior of galliform birds is atypical because the chicks are precocial, requiring relatively little parental attention, and because the males provide little or no parental care. Another well-studied group, the Columbiformes, provide biparental care, but doves and pigeons secrete prolactin to stimulate maturation and secretions of the highly specialized crop gland, an adaptation for providing nutrition to the hatchlings that is not found in any other order of birds. Thus, control of prolactin secretion and parental behavior in these domesticated species could differ from that in the majority of other bird species. The Role of Prolactin and Species Differences A rise in prolactin is associated with the onset or maintenance of egg incubation and care of young in a number of free-living passerine species (Goldsmith, 1991; Buntin, 1996). The rise may occur abruptly at the time of egg laying and incubation, or prolactin may rise more slowly and not peak until later in incubation. Some of these differences may result from selection for different reproductive strategies associated with clutch size, laying interval and when incubation normally begins within the laying sequence. Prolactin levels usually decline rapidly after the chicks hatch in species with precocial young, and the presence of the chicks can modify this rate of decline (Dittami, 1981; Opel and Proudman, 1989). Prolactin levels generally decline more slowly in species with altricial young, presumably because parental brooding is required for chick survival, just as it is for embryo survival. Prolactin levels often begin to decline only after the chicks achieve thermal independence and do not require constant brooding (Goldsmith, 1991). In some species with altricial young, prolactin levels decline more rapidly relative to chick maturity that in others (Silverin and Goldsmith, 1983). This suggests that the waning of importance of page 2
prolactin and the transition to other factors that control behavior, including sensory feedback from the chicks themselves has been subject to selection. Despite the strong correlation between prolactin and parental behavior, the extent to which prolactin determines parental behavior or whether prolactin rises as a consequence of the behavior is not clear. Even if prolactin controls parental behavior, it is not apparent whether prolactin is necessarily required for the initiation of incubation behavior or just its maintenance. In the Adelie penguin (Pygoscelis adelie) prolactin levels reach their maximum only about halfway through incubation, despite the fact that 100% attentiveness at the nest is required as soon as the eggs are laid to avoid egg freezing and loss of eggs to predators. Prolactin levels do not begin to decrease significantly until almost two weeks after hatching, at about the time the chicks form crèches and no long require constant brooding ( and Bucher, in press). In king penguins (Aptenodytes patagonicus) the chicks remain in the colony for many months and, compared to non-breeding adults, prolactin is elevated in the parents who infrequently return to the colonies to feed the chicks (Cherel et al., 1994) One way to study the cause and effect relationship between prolactin and parental behavior is through manipulative experiments. In some species artificial extension or termination of the incubation period affects prolactin levels, supporting the hypothesis that performance of incubation influences prolactin secretion (Silverin and Goldsmith, 1984; Oring et al., 1988). Similarly, manipulation of chick ages can influence prolactin levels in brooding birds, but only within certain limits (Silverin and Goldsmith, 1990). In other species, prolactin levels seem to be determined by an endogenous schedule or by daylength, relatively independently of the bird's exposure to nest and eggs (Ebling et al., 1982; Hector and Goldsmith, 1985). On the other hand, as nest deprivation studies in domesticated species indicate, prolactin levels need not necessarily be elevated for incubation behavior to be expressed. Broody females deprived of their nest show a decline in prolactin levels, but will begin incubating as soon as returned to their nest, even though prolactin levels do not rise again until later (El Halawani et al., 1980; Lea and Sharp, 1989; Zadworny et al., 1985)). Such behavioral effects, however, could be attributed to a carry-over effect of the previous prolactin elevation. Other manipulative experiments to alter hormone milieus and examine behavior have been carried out primarily with domestic species. Induction of brood patch formation and broody behavior have been achieved in poultry species with appropriate combination of steroid and prolactin treatment (El Halawani et al., 1985) and in caged budgerigars (Melopsittacus undulatus) (Hutchison, 1975). Free-living female willow ptarmigan (Lagopus lagopus) receiving supplement prolactin from implanted osmotic pumps displayed more intense defense of chicks compared to controls, and chick survival was also increased (Pedersen, 1989). Additional experimentation with wild birds awaits less invasive ways to alter prolactin levels. Variation in the intensity of parental care displayed is often not tightly correlated with variation in the level of prolactin ( Silverin and Goldsmith, 1984; Janik and Buntin, 1985; Ketterson et al., page 3
1990; et al., 1991; Buntin et al., 1996; Schoech et al., 1996), suggesting that the level of parental effort is not modulated in any precise way by the level of prolactin secretion (or viceversa). In Harris hawks (Parabuteo unicinctus) the effort that parents expend to rear the young varies with group size because other members of the group help to feed the chicks (see below). Despite the reduction in parental effort in large groups, there is no relationship between prolactin in the breeding adults and group size ( et al., 1991). Likewise, there is no relationship between prolactin and chick feeding rate in Mexican jays (Aphelocoma ultramarina) ( and Brown, unpubl. data, but see Schoech et al. 1996). Elevated prolactin may be necessary for the display of parental behavior, but parental behavior is not fine-tuned by variations in prolactin level. Levels of prolactin are usually higher in females than in males, whether or not the male participates in incubation (Dawson and Goldsmith, 1982; Hiatt et al., 1987). For example, prolactin in incubating female Harris hawks is more than double the level found in the males, even though the latter participate in incubation ( et al., 1991). In Mexican jays, peak prolactin levels are only about 20% higher in females than in males (Brown and, 1998), even though the males do not incubate, but rather do feed the incubating female who seldom leaves the nest. Higher levels in females could be due to synergism with estrogen or progesterone. Among species in which the male incubates more than the female however, prolactin levels are higher in males than in females ( Oring et al., 1986; Oring et al., 1988; Gratto-Trevor et al., 1990). In these species, testosterone levels are higher in the males than in the females, so the androgens rather than estrogens may play a role in prolactin priming. In general, high levels of testosterone are thought to be incompatible with the display of male parental behavior. Male birds that engage in parental behavior may show elevated levels of testosterone during courtship and mating stages, but these levels generally plummet when the birds enter the parental phase of reproduction (Wingfield et al., 1990). Anti-androgens can bring about a premature onset of incubation (Oring and Fivizzani, 1991). Furthermore, androgen supplementation is known to disrupt parental behavior in several free-living species ( Silverin, 1980; Hegner and Wingfield, 1987; Oring et al., 1989; Ketterson et al., 1992). Testosterone does not necessarily block the display of parental behavior, but rather seems to increase the likelihood that the birds will engage in others non-parental behaviors (e.g. courtship or territorial defense) at the expense of parental behavior. In wild-caught bobwhite quail (Colinus virginianus) used as foster fathers in a reintroduction program in southern Arizona, those males which accepted chicks after forced confinement with them had testosterone levels that were less than half those of males that did not show alloparental behavior ( and Dobrott, 1993). Anti-androgens did not, however, affect this behavior. Essentially continuous tactile stimulation from the eggs is required to maintain elevated prolactin and broodiness in poultry species (El Halawani et al., 1980; Hall et al., 1986; Hall, 1987; Sharp et al., 1988). Visual stimuli and previous breeding experience also affect the propensity for birds to show parental behavior. The absolute necessity for such sensory input for the maintenance of prolactin secretion and incubation behavior is demonstrated by sensory deprivation experiments page 4
in which the brood patch is either denervated or anaesthetized. Incubating birds deprived of sensory stimulation for nest and eggs promptly abandon their nests (Book, 1991). These manipulative types of experiments have not been carried out in any wild bird. However, in many species in which both members of the pair incubate, one bird can be absent from the nest for hours to days, but still maintain the urge to return to the nest and incubate (Hector and Goldsmith, 1985; Lea et al., 1986). In Adelie penguins, the females go to sea to feed after the second egg is laid and may not return for one to three weeks. When they return, however, their prolactin levels are at their peak and they display a very strong urge to incubate ( and Bucher, in press). Whether that prolactin secretion is cued by an external cycle like photoperiod or is the result of an endogenous program associated with breeding is not known. Considerable data on domesticated species indicates that the efficacy of prolactin to influence parental behavior may depend on synergistic interaction with gonadal steroids, especially estrogens and progesterone (Buntin, 1996). For example, induction of brood patch formation and broody behavior can be achieved only if prolactin treatments are accompanied by steroids (Jones, 1971). This hypothesis is difficult to address in wild birds because steroid hormones are already elevated in breeding birds. Non-breeding birds that show parental-like behavior toward eggs and chicks that are not their own (either referred to as alloparental behavior or helping behavior) are a possible exception. In poultry species forced confinement of non-breeding adults with chicks can induce parental behavior even in the absence of any change in prolactin (Richard-Yris et al., 1995). Group-living species in which non-breeders are exposed to begging young constitute a natural example of such a social cue. In most birds the display of parental behavior proceeds in a cyclic manner after the mating and egg production stages. That is not the case in cooperative breeders in which extra birds assist the breeding pair in raising the young. These helpers seldom incubate, but usually feed and defend the chicks. They are often older offspring of the breeding pair, but in some species may be unrelated to the birds they help. Variations of this behavior occurs in at least 222 species of birds; the phenomenon is taxonomically widespread among altricial species (Brown, 1987). Elevated prolactin is found in helpers at the time they are engaging in this alloparental behavior. In the Harris Hawk prolactin levels in the breeders decline immediately after the eggs hatch, but at the same time it rises in the adult-plumaged male helpers that bring more food items to the nestlings than any other group members ( et al., 1991). These same helpers displayed high levels of testosterone earlier in the season, in contrast to other group members who do not display elevated prolactin (Mays et al., 1991). This suggests that the sex steroids may prime prolactin release and parental behavior even in birds that are not the primary breeders in the group. Paternity exclusion studies in other species suggest that many of these supposed non-breeding males may actually achieve some successful copulations and fertilizations (Westneat et al., 1990). In the two other cooperatively-breeding species in which prolactin has been measured (Florida scrub-jay, Aphelocoma c. coerulescens, and Mexican jay), prolactin is also elevated in helpers during the breeding season (Schoech et al., 1996; Brown and, 1998). Many of these helper birds are unlikely to have been sexually active since they are often yearlings. In these species, page 5
however, prolactin in all the non-breeding helpers is elevated well before begging young are present. This argues against the hypothesis that elevated prolactin and parental behavior in helpers occurs purely as a response to confinement with begging young (Jamieson, 1989). Elevated prolactin in helpers may have evolved as a specific physiological adaptation to facilitate care of young in these cooperatively breeding species. Prolactin in the jay species with helpers is significantly higher than in a closely related, sympatric jay that does not display helping behavior (Brown and, 1998). Control of Prolactin Secretion A number of chemicals are known to affect avian prolactin secretion in domesticated species. Vasoactive intestinal peptide (VIP) is a potent prolactin releasing hormone, whereas dopamine is a prolactin inhibiting hormone. The effectiveness of these hypothalamic factors in controlling pituitary prolactin release appears to depend strongly upon the stage of the breeding cycle (El Halawani et al., 1991; Youngren et al., 1995; Youngren et al., 1996). VIP acts as a prolactin releasing factor in wild birds as well ( and Patrick, submitted), suggesting that the underlying neural control of prolactin secretion is similar in all avian species. There may be species differences in whether the control system is seasonally sensitive, that vary with whether a species is photoperiodic or not. VIP treatment in Mexican jays outside the normal breeding season causes a rise in prolactin, but prolactin does not reach levels found in breeding jays. In contrast VIP treatment of non-breeding zebra finches (Poephila guttata) results in maximally high prolactin levels. Desert-adapted, Australian zebra finches are not photoperiodic and will breed whenever conditions (generally access to food and water) are permissive ( and Priedkalns, 1985). There is also evidence for tonic secretions of pituitary gonadotropins in zebra finches (Farner and Serventy, 1960) rather than the large seasonal adjustments that are found in most birds. In this species the anterior pituitary may be maximally sensitive to VIP at all times rather than depending on the time of year. Pharmacological and immunological treatments that block prolactin secretion will limit broody behavior in domestic species, but have not yet been shown to be effective in any wild birds. Block of serotonin synthesis with p-chlorophenylalanine suppresses prolactin secretion in turkeys (El Halawani et al., 1980), but not in Mexican jays ( and Patrick, submitted). Active or passive immunization against VIP blocks prolactin secretion in domesticated species (Sharp, 1997). Passive immunization against VIP in zebra finches and blue jays (Cyanocitta cristata) does not decrease prolactin more than is found in controls ( and Patrick, submitted), so it is not yet possible to say to what extent prolactin secretion in wild species can be manipulated via immunological methods. Conclusions A variety of social, environmental, physiological and experiential factors appear to influence parental behavior; the most clear-cut factor being elevated prolactin (Buntin, 1996). Prolactin secretion and parental behavior appear to be mutually reinforcing such that is it difficult to tease apart cause and effect. The distinction for wild birds may have little biological meaning. It may be page 6
that multiple, redundant mechanisms have evolved to reinforce parental behavior because of its direct tie to fitness. The general similarity between domesticated and wild birds in the importance of prolactin suggests that the process of domestication has had little effect on this process and wild birds can serve as useful models for the control of parental behavior in domesticated species. For example, brood parasites lay large numbers of eggs and exhibit no parental behavior past egg laying. Despite this fact, one obligate brood parasite, the brown-headed cowbird (Molothrus ater) displays a seasonal rise in plasma prolactin (Dufty et al., 1987). This suggests that sensitivity to prolactin can be decreased and the behavior eliminated, probably by way of decreased binding activity within the brain (Ball et al., 1988). We have a reasonable description of the diversity of patterns in prolactin secretion and parental behavior across all bird species, but as yet there is little general theory that addresses the adaptive significance of these differences. Additional studies of free-living birds under a variety of ecological conditions will continue to provide lessons about the hormonal control of parental behavior. Acknowledgement Parts of this work were supported by NSF grants IBN-9211581 and OPP-93-17356. References Ball, G.F., Dufty, A.M., Goldsmith, A.R., and Buntin, J.D. (1988) Autoradiographic localization of brain prolactin receptors in a parental and non-parental songbird species. Society for Neuroscience, Abstracts 14: 88 Book, C.M. (1991) Brood patch innervation and its role in the onset of incubation in the turkey hen. Physiology and Behavior 50: 281-285 Brown, J.L. (1987). Helping and Communal Breeding in Birds: Ecology and Evolution, Krebs, J.R.a.C.-B., T., ed. Princeton University Press,Princeton, NY Brown, J.L., and, C.M. (1998) Prolactin and helping in birds: has natural selection strengthened helping behavior? Behavioral Ecology 0: 000-000 Buntin, J.D. (1996) Neural and hormonal control of parental behavior in birds. Advances in the Study of Behavior. 25: 161-213 Buntin, J.D., Hnasko, R.M., Zuzick, P.H., Valentine, D.L., and Scammell, J.G. (1996) Changes in bioactive prolactin-like activity in plasma and its relationship to incubation behavior in breeding ring doves. General and Comparative Endocrinology 102: 221-232 Cherel, Y., Gilles, J., Handrich, Y., and LeMaho, Y. (1994) Nutrient reserve dynamics and energetics during long-term fasting in the king penguin (Aptenodytes patagonicus). Journal of Zoology, London 234: 1-12 Dawson, A., and Goldsmith, A.R. (1982) Prolactin and gonadotrophin secretion in wild starlings (Sturnus vulgaris) during the annual cycle and in relation to nesting, incubation, and rearing young. General and Comparative Endocrinology 48: 213-221 Dittami, J. (1981) Seasonal changes in the behavior and plasma titers of various hormones in barheaded geese, Anser indicus. Zeitshrift für Tierpsychologie 55: 289-324 page 7
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