Relationships of Steroid Hormones and Polygyny to Territorial Status, Breeding Experience, and Reproductive Success in Male Red-Winged Blackbirds

-We collected 354 blood samples from territorial and nonterritorial male Redwinged Blackbirds (Agelaius phoeniceus) to determine plasma levels of testosterone (T) and corticosterone (B) of a polygynously breeding bird, and to determine the potential influences of steroid hormone levels on obtaining breeding territories. In contrast to monogamous species, we found no peak in average T levels early in the breeding season and a five-weeklong high plateau in T levels during the period when most nests were initiated. These endocrinologic characteristics may result from the long breeding season and resource defense polygyny of Red-wings. Territory owners had higher T levels during the breeding season than adult floaters. Subadult floaters had the lowest levels. Also, territory owners generally had the highest circulating levels of corticosterone during most of the breeding season. This implies greater energetic demands and stress on owners than on floaters. During early April the T levels of males for which we had complete breeding and territorial history information correlated significantly with their annual fledging success, and males with more breeding experience tended to have higher peak T levels. There was also a positive correlation between B levels in early April and eventual fledging success. Circulating levels of steroid hormones may affect territory ownership and reproductive success in this species. Received 17 February 1988, accepted 24 August 1988. STEROID hormones influence the reproductive behavior of birds and other animals (for reviews see Sossinka et al. 1980, Balthazart 1983, Wingfield et al. 1987). The interrelationships among environmental stimuli, hormone levels, and behavior, however, are poorly understood. Free-ranging birds have only recently been monitored for circulating levels of steroid hormones and associated reproductive behavior (e.g. Wingfield and Farner 1978, Silverin 1983, Wingfield 1985a, Dufty and Wingfield 1986, Hegner and Wingfield 1986a, b). Most of these studies have focused on monogamous species. Testosterone (T) levels stimulate certain behaviors such as singing (Nottebohm 1981) and are directly related to the intensity of shortterm aggressive behavior. Testosterone may not trigger aggression, but may facilitate expression of the behaviors involved at high frequency and intensity (Wingfield et al. 1987). When territorial males are "challenged" by conspecific males, T levels rise as they defend their territories or mates (the "challenge hypothesis"; Wingfield 1985a, in press; Wingfield et al. 1987). In the monogamous songbird species that have been examined, this process characteristically results in circulating T levels that peak during territory establishment, peak again during a period of mate-guarding, and then decline sharply (Wingfield and Moore 1986, Wingfield et al. 1987). The seasonal profiles of testosterone in males of bigamous Pied Flycatchers (Ficedula hypoleuca; Silverin and Wingfield 1982) and brood parasitic Brown-headed Cowbirds (Molothrus ater; Dufty and Wingfield 1986) departed significantly from those typical of monogamous breeders. In these species, T levels were elevated for prolonged periods, associated in time with sequential or continuous male mateguarding behavior. The Red-winged Blackbird (Agelaius phoeniceus) is strongly polygynous. Males maintain territories, guard multiple mates, and defend nests from predators for two to four months in the spring. Individual males acquire females over long time periods and harems differ strikingly in size. Because of high nest-predation rates and renesting by females, males often have nests in several different stages of the breeding cycle at the same time and over many weeks. Therefore, the seasonal profiles of steroid hormones for this species should be valuable for testing hypotheses about relationships among 107 The Auk 106: 107-117. January 1989 This content downloaded from 207.46.13.172 on Sat, 15 Oct 2016 04:19:13 UTC All use subject to http://about.jstor.org/terms 108 BELETSKY, ORIANS, AND WINGFIELD [Auk, Vol. 106 hormone levels, behavior, and mating systems, particularly those that bear on testosterone and aggression (Harding 1981; Wingfield 1984, in press; Wingfield et al. 1987). Male Red-wings usually do not obtain territories until they are two or more years old. Therefore, in any given year, there is a sizeable floating population of nonbreeders whose hormone levels can be compared with those that hold territories. Within-season reproductive success of males is strongly correlated with harem size (Beletsky and Orians 1987, Orians and Beletsky 1989), offering the possibility of relating hormone levels to determinants of reproductive success. We studied hormone levels in a population of Red-wings that had been monitored intensively for breeding behavior and breeding success for over a decade. Our purposes were to establish the basic seasonal patterns of steroid hormone levels in territorial and nonterritorial males, to test whether these patterns conformed to predictions from the "challenge hypothesis" of T secretion (Wingfield et al. 1987, Wingfield in press), and to examine relationships between hormone levels and reproductive success. We have now elucidated the relationships among plasma testosterone and corticosterone (B) levels and territorial status, documented average circulating levels of T and B for a broad range of individuals over the course of a breeding season, and related steroid hormone levels to reproductive success of breeding males. Corticosterone levels were measured as an indicator of stress (e.g. Harvey et al. 1984; Wingfield 1984, 1985b). We divided male Red-wings in the population into three territorial classes. Adult territory owners were males at least two years old that successfully held territories. Adult nonterritorial floaters were males at least two years old that did not have territories. Floaters remained in particular areas over prolonged periods, attempting to acquire territories. Adult floaters often intruded on occupied territories. Sometimes they persistently challenged established males for ownership; they quickly filled territory vacancies when they occurred; and they attempted to copulate with unguarded females. Subadult floaters were one-year-old, nonterritorial males. They weighed, on average, about 10% less than adults and had a distinctive plumage (brown primaries and orange epaulet feathers as opposed to the jet black and red-epauleted adults). They had functional testes (Payne 1969, Wiley and Hartnett 1976). Each year a few subadults at the study site succeeded in establishing territories and attracted at least one mate, but they rarely produced offspring. Most remained in small groups feeding and roosting together. Due to their roving nature, the behavior of floaters is not well understood in this and other species. We predicted that territory owners would have the highest plasma T levels during the breeding season, and that adult floaters, the most aggressive territorial challengers, would have higher levels than subadult males. The predictions were based on the observation that circulating levels of T are positively correlated with intensity of aggressive behavior in Red-wings and other birds (Searcy and Wingfield 1980, Harding 1981, Balthazart 1983, Wingfield 1983, Moore 1984) and that territorial dominance is clearly linked with aggressive behavior. Corticosterone is thought to regulate adaptive changes in behavior when individuals are exposed to stressful environmental conditions (Wingfield and Silverin 1986, Wingfield in press). During a breeding season without major storms or nutritional stresses, only one of the three classes of male Red-wings (territory owners) are likely to be regularly stressed. Floaters probe for territorial opportunities but they typically withdraw when the owner approaches. Floaters forage primarily in communal, undefended areas where there are few agonistic interactions. Territory owners, on the other hand, patrol and defend their territories many times per day. Owners continually advertise to attract mates; they court, chase, and guard their multiple mates; and they defend their nests from a variety of predators. There is a temporal tradeoff between territorial activities and foraging off territory (Ydenberg and Krebs 1987). In fact, body mass of most territorial males declines as breeding progresses (Orians and Beletsky unpubl. data). Therefore, we predicted that corticosterone levels of territorial males would be consistently higher than those of nonterritorial males.