Androgens and Mating Systems: Testosterone-induced Polygyny in Normally Monogamous Birds

-Recent investigations of the plasma profiles of testosterone (T) in free-living birds suggest that circulating levels of T during the reproductive cycle remain elevated longer in males of polygynous species than in males of monogamous species. When the hormonal profile of polygynous males is mimicked by the administration of subcutaneous implants of T to males of monogamous species, thus maintaining plasma levels of this androgen at high vernal levels, frequencies of territorial aggression and courtship behavior remain elevated, resulting in a marked increase in the size of the territory. A substantial number of T-implanted males also become polygynous, attracting two and sometimes three females to settle on their enlarged territories. These data suggest strongly that the nature of avian mating systems is regulated proximately by temporal patterns of hormone secretion. Received 2 December 1983, accepted 27 April 1984. IN the early spring, males of many passerine birds establish breeding territories to which they then attract a mate or mates. The seasonal development of behaviors associated with the establishment of a territory, courtship, and mate-guarding are regulated by the steroid hormone testosterone (T) (e.g. Hutchison 1978, Farner and Follett 1979, Wingfield and Farner 1980a, Adkins-Regan 1981, Moore 1984). Circulating levels of T in males are elevated throughout the spring, reaching a maximum when females are ovulating and when most copulations occur (Wingfield and Farner 1980a; Wingfield 1980, 1983). In monogamous species there is a rapid decline in plasma levels of T (Wingfield 1980, 1983; Wingfield and Farner 1980a), accompanied by a reduction of territorial and sexual behavior, as soon as the female begins incubation. In polygynous species, however, circulating T remains elevated throughout incubation [e.g. Red-winged Blackbird (Agelaius phoeniceus), W. A. Searcy pers. comm.] or at least until the final mate has begun incubation [e.g. Pied Flycatcher (Ficedula hypoleuca), Silverin and Wingfield 1982]. In the weakly polygynous Western Meadowlark (Sturnella neglecta), plasma levels of T do decline as incubation ensues but then increase for a second time when females are producing a second clutch (Wingfield and Farner 1980b). Monogamous males of captive populations of turtle doves (Streptopelia spp.), however, also manifest an elevation of T during the courtship phases of subsequent broods (Feder et al. 1977). This is unlike most monogamous species, such as the White-crowned Sparrow (Zonotrichia leucophrys; Wingfield and Farner 1978a, b, 1980a), Eurasian Blackbird (Turdus merula; Schwabl et al. 1980), and Song Sparrow (Melospiza melodia; Wingfield 1984a), in which plasma levels of T remain depressed, even though up to four clutches may be produced within a single season. In addition, it has been shown that in the monogamous wild Mallard (Anas platyrhynchos) plasma levels of T decrease as soon as the female is incubating. In domesticated and semidomesticated forms of Mallards, however, the mating system becomes promiscuous, plasma levels of T remaining elevated for longer during the breeding period (Donham 1980, Haase and Donham 1980). Although caution should be exercised in comparing plasma profiles of hormones of truly wild and domesticated forms of the same species, these data do support the hypothesis that, in monogamous males, plasma T is elevated only early in the season when territories and pair bonds are established, whereas, in polygynous forms, plasma T is elevated for longer periods that may overlap the parental phase. This communication reports the effects of mimicking the hormonal profile of polygynous species by administering subcutaneous implants of T to males of monogamous species and thus maintaining plasma levels of this androgen at high springtime levels. MATERIALS AND METHODS Experimental subjects and study sites. -In the spring of 1979, an investigation into the behavioral effects 665 The Auk 101: 665-671. October 1984 This content downloaded from 207.46. 13.83 on Fri, 21 Oct 2016 04:47:45 UTC All use subject to http://about.jstor. org/terms 666 JOHN C. WINGFIELD [Auk, Vol. 101 of experimentally altered temporal patterns of T secretion in male White-crowned Sparrows (Zonotrichia leucophrys pugetensis) was initiated at a study site near Hart's Lake, Pierce County, Washington (45? N). Freeliving populations of this race of White-crowned Sparrow are known to be primarily monogamous (Blanchard 1941, Lewis 1975). In the spring of 1981 this experiment was repeated with free-living male Song Sparrows (Melospiza melodia) on the grounds of the Rockefeller University Field Research Center and adjacent lands of the Cary Arboretum of the New York Botanical Society, Millbrook, New York (42? N). Song Sparrows are monogamous, although occasional instances of polygyny are reported (Nice 1943, Smith and Roff 1980). Hormone implants and sampling procedures. -To alter the temporal pattern of circulating T levels, eight territorial male White-crowned Sparrows were given a subcutaneous implant of crystalline T packed into 20-mm lengths of Silastic tubing (internal diameter 1.47 mm, external diameter 1.96 mm; Dow Corning, Midland, Michigan). Controls (n = 9) were given empty implants at a second site some 8 km distant. In the second experiment, a group of 8 territorial male Song Sparrows were given identical implants of T, and in an area 1 km distant a second group of 8 males were given empty implants as controls. All implanted birds were surrounded by untreated but territorial males, and all implants were administered early in spring as territories and pair bonds were being established. Birds were captured in Japanese mist nets or in Potter traps baited with seeds. Blood samples were collected immediately after capture and before implantation. Sparrows were banded with a U.S. Fish and Wildlife Service aluminum band and a unique combination of colored plastic leg bands for identification of individuals during subsequent behavioral observations. All females captured were also color banded. At each capture, body mass was measured to the nearest 0.1 g, fat depot in the furculum and abdomen was assessed on an arbitrary scale, and wing length was recorded to the nearest millimeter. All of these sampling procedures have been described in detail by Wingfield and Farner (1976, 1978a). At intervals throughout the breeding season, experimental birds and controls were recaptured and further samples were collected. Implants were checked at each capture and, in experimentals, T implants were replaced if the original implant was half empty. Behavioral observations. -Birds were identified by color-band combinations during regular censuses at least once a week. The bird's location and interactions with conspecifics were also noted. These observations were divided equally between experimental and control sites. Territory size was measured after boundaries had been established (May-July) as follows: tape-recorded songs of Song Sparrows (territory size was not assessed for implanted Whitecrowned Sparrows) were played to experimental and control males, the position of singing perches was noted on a detailed map, and the area circumscribed by the perches was measured in square meters. Because only singing and display perches were used to identify territory boundaries, these data represent conservative estimates of territory size. Polygynous associations were indicated by the presence of two or more nests within a territory and by repeated observations of breeding females, identified by color bands, associating with a particular male or carrying food to young on an observed male's