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Temporal Patterns of Territorial Behavior and Circulating Testosterone in the Lapland Longspur and Other Arctic Passerines1

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Temporal Patterns of Territorial Behavior and Circulating Testosterone in the Lapland Longspur and Other Arctic Passerines1 AMER. ZOOL., 35:274-284 (1995) Temporal Patterns of Territorial Behavior and Circulating Testosterone in the Lapland Longspur and Other Arctic Passerines1 KATHLEEN HUNT, JOHN C. WINGFIELD, LEE B. ASTHEIMER2, WILLIAM A. BUTTEMER,2 AND THOMAS P. HAHN3 Department of Zoology, NJ-15, University of Washington, Seattle, Washington 98195 SYNOPSIS. We studied territorial aggression in relation to circulating tes- tosterone levels in free-living birds of four species in northern Alaska. The Lapland longspur, Calcarius lapponicus, is an abundant breeding Downloaded from https://academic.oup.com/icb/article/35/3/274/167719 by guest on 02 October 2021 passerine on the arctic tundra. Unlike many passerines at lower latitudes, male Lapland longspurs do not defend a "multiple-purpose territory" that serves to provide nest sites, food and shelter. Rather, after arrival on the breeding grounds, they perform aerial display flights over a loosely denned "nest area" for a very brief period of two days or so, showing tolerance of other males. This song display may be involved in courtship. During this phase, male longspurs show a brief and pronounced peak in circulating testosterone levels, and are not aggressive toward simulated territorial intrusions (STIs). Males then "guard" their sexually receptive mates for about ten days, during which they are highly aggressive toward STIs, but do not sing as much. During the next phase, incubation, the males become very tolerant of conspecific males. Their circulating testosterone levels decline to baseline levels, and they generally do not sing or display aggres- sion in response to STIs. Three other passerines, the white-crowned spar- row, Zonotrichia leucophrys gambelii, American tree sparrow, Spizella arborea, and savannah sparrow, Passerculus sandwichensis, show patterns of territorial aggression typical of species studied at lower latitudes. Well- defined territories are defended for several weeks, during which there is a prolonged peak in plasma concentrations of testosterone. These three species continue to sing and display aggression even late in the season, unlike the longspurs. The peak of testosterone in the longspurs occurs simultaneously with the peak in song display, while in mid-latitude species it occurs with the peak in reproductive aggression. These data suggest that the interrelationship of testosterone and aggression in Lapland longspurs may be different from that of passerines with multiple-purpose territories, and may be related to the constraints of breeding in the open arctic tundra. INTRODUCTION intensity and duration from species to spe- Male passerine birds commonly show cies. For instance, early in the breeding sea- certain breeding behaviors that vary in son> males typically spend much time sing- ing, courting females, and defending their territory from rival males, and will reduce 1 From the Symposium Endocrinology of Arctic Birds or cease these activities later in the season. and Mammals presented at the Annual Meeting of the Such behaviors are important for synchro- American Society of Zoologists, 27-30 December 1993, nizing the male's and female's physiology at Los Angeles, California. ,,", . c ci * \- e .L » Present address of Lee B. Astheimer and William and behavior, from final maturation of the A. Buttemer is: Department of Biomedical Research gonads to the shift from sexual to parental and Department of Biological Sciences, University of behavior. These complex behavioral inter- Wollongong, Wollongong, New South Wales 2500, actions have been shown to have an inti- A mat e "prestnt address of Thomas P. Hahn is: Department u relationship with Steroid hormones, of Psychology, Johns Hopkins University, Baltimore, Such as testosterone (I), estradlOl, and their Maryland 21218. metabolites (e.g., Balthazart, 1983; Harding 274 TERRITORIALITY IN ARCTIC PASSERINES 275 et al., 1988; Wingfield and Ramenofsky, restricted nesting cycle with the more pro- 1985; Wingfield and Moore, 1987). Fur- tracted breeding cycle common in lower- thermore, the temporal patterns of circu- latitude species raises a number of ques- lating hormone levels {e.g., testosterone) in tions. Do breeding behaviors (such as ter- different species appear to be linked to ritorial and mate-guarding aggression, song, breeding strategies and mating systems, sug- and courtship) have different intensities or gesting a broad interrelationship of behav- duration in birds that must complete breed- ioral ecology and endocrine mechanisms ing in the fleeting arctic summer? Do cir- (Wingfield et al., 1990). However, most culating testosterone levels show a pattern investigations on the interrelationships of that is different in any way {e.g., in the Downloaded from https://academic.oup.com/icb/article/35/3/274/167719 by guest on 02 October 2021 testosterone and aggression have focused on amplitude, timing, or behavioral correlates temperate zone species in which the breed- of the seasonal T peak) from that seen in ing season may be protracted {i.e., 2-5 lower-latitude species? If so, what aspects months). None have addressed the tempo- of the Arctic might be most important in ral progression and integration of repro- exerting the selective pressures that result ductive events in the Arctic, where breeding in different breeding strategies? Here we seasons are usually only 4-5 weeks. compare the testosterone-behavior inter- Species from mid-latitudes, such as the relationships of a truly arctic passerine, the Puget Sound white-crowned sparrow Lapland longspur, with other passerines that {Zonotrichia leucophrys pugetensis) and song breed both in the Arctic and at lower lati- sparrow {Melospiza melodia), have multi- tudes. As we are comparing several different ple-purpose territories that males defend aspects of behavior, we have arranged this throughout the breeding season. Territorial paper by topics. We first discuss the natural defense includes singing, patrolling, and history of our four species, and then describe agonistic encounters with challenging males. methods and results for temporal patterns During aggressive encounters, the territorial of testosterone, and then for aggressive male approaches the intruder and gives behavior. Finally, we compare the four spe- songs, threat postures, short flights (flutter- cies and discuss the ecological context of ing wings and short flights from perch to these hormone-behavior relationships. perch around the intruder), and direct attacks, remaining within 5 m until the NATURAL HISTORY intruder is expelled from the territory (see General methods Wingfield and Moore, 1987; Wingfield and Hahn, 1994). Note that males also use song We studied a population of Lapland long- as an advertisement or courtship signal to spurs {Calcarius lapponicus, "longspurs"), attract mates. These behaviors have been Gambel's white-crowned sparrows {Zono- shown to be activated and prolonged by tes- trichia leucophrys gambelii), American tree tosterone^., Balthazart, 1983; Harding e< sparrows {Spizella arborea) and savannah al., 1988; Wingfield and Moore, 1987; sparrows {Passerculus sandwichensis) at Wingfield, 1994). Once plasma levels of tes- Toolik Lake (68°38'N, 149°38"W), Alaska, tosterone decline at the end of the breeding during the summers of 1989-1994. Birds season, then high levels of spontaneous were captured in Potter traps baited with aggression, and of courtship-related activi- seeds or in Japanese mist nets, and each ties, also decline (see Nowicki and Ball, individual (except for savannah sparrows) 1989). These behaviors are typical of pas- was banded with a unique combination of serines breeding at northern mid-latitudes. color bands for subsequent observation and Most species that have been studied breed identification in the field. In each year, we in wooded or semi-open habitat (shrubs and identified mated pairs and observed behav- thickets), and many maintain multiple-pur- ioral patterns and general reproductive biol- pose territories for several months. ogy- Arctic birds, in contrast, have a very short Natural history of the Lapland Longspur breeding season. Comparison of hormone- The Lapland longspur is a small passerine behavior adaptations in this temporally that breeds throughout much of the Arctic 276 K. HUNT ET AL. tundra region. It has a circumpolar distri- residents. They will also congregate at bution and is thought to be the most abun- unusually rich sites for food, such as at our dant arctic breeding bird (Bent, 1968). Males seed-baited trap sites. arrive on the breeding grounds in mid-May Clearly, male Lapland longspurs do not (e.g., Irving, 1960) and within a few days defend a classical multiple-purpose terri- they show display flights accompanied by tory, and instead appear to show a brief song over an apparent "territory" (or at least series of territorial behaviors that begin with they show these aerial displays over the same the aerial displays and songs, and finish with small patch of ground, about 50-100 m in mate-guarding behavior. Our general obser- diameter; L. B. Astheimer and K. Hunt, vations of the Lapland longspurs at Toolik Downloaded from https://academic.oup.com/icb/article/35/3/274/167719 by guest on 02 October 2021 unpublished observations). A displaying Lake concur with data published for this male typically flies up to a height of about species breeding at Barrow, Alaska (Custer 50 m, holds his wings out, and glides down- and Pitelka, 1977); Bylot Island, Northwest ward in a large spiral while singing several Territories, Canada (Drury, 1961) and
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