UC Davis UC Davis Previously Published Works Title Male territorial aggression and androgen modulation in high latitude populations of the Sooty, Passerella iliaca sinuosa, and Red Fox Sparrow, Passerella iliaca zaboria Permalink https://escholarship.org/uc/item/9hh8q77g Journal Journal of Ornithology, 151(1) ISSN 1439-0361 Authors Wacker, Douglas W. Coverdill, Alexander J. Bauer, Carolyn M. et al. Publication Date 2010 DOI 10.1007/s10336-009-0428-9 Peer reviewed eScholarship.org Powered by the California Digital Library University of California J Ornithol (2010) 151:79–86 DOI 10.1007/s10336-009-0428-9 ORIGINAL ARTICLE Male territorial aggression and androgen modulation in high latitude populations of the Sooty, Passerella iliaca sinuosa, and Red Fox Sparrow, Passerella iliaca zaboria Douglas W. Wacker Æ Alexander J. Coverdill Æ Carolyn M. Bauer Æ John C. Wingfield Received: 22 October 2008 / Revised: 11 March 2009 / Accepted: 25 May 2009 / Published online: 26 June 2009 Ó The Author(s) 2009. This article is published with open access at Springerlink.com Abstract The Fox Sparrows, Passerella iliaca, include subarctic Red Fox Sparrows had slightly higher circulating multiple groups and subspecies distributed at several lati- androgen levels (2.29 ng/ml) than arctic males (1.10 ng/ml) tudes from the Alaskan arctic to the southwestern United in the mid–late breeding season. However, androgen levels States. As such, this species represents a potential model for were not correlated with blood collection time after a social investigating latitudinal variation in androgen secretion and challenge in either group, suggesting that neither arctic nor aggressive territoriality in male passerines. Breeding male subarctic males up-regulate androgen secretion during the Fox Sparrows from two subspecies within two groups, the mid–late breeding period. Arctic males spent more time Sooty Fox Sparrow, P. i. sinuosa, and the Red Fox Sparrow, within 5 m of a decoy and sang less than subarctic males P. i. zaboria, were assessed for aggressive territoriality and during an STI in the mid–late breeding season. These find- androgen responsiveness at multiple latitudes in arctic and ings demonstrate that the Fox Sparrow is a tractable model subarctic Alaska. Subarctic Sooty Fox Sparrows had higher for investigating the latitudinal regulation of aggressive circulating androgen levels in the early (8.54 ng/ml) versus territoriality and androgen responsiveness in passerines. mid–late breeding season (2.44 ng/ml). Males in the mid– late breeding season did not up-regulate androgen secretion Keywords Passerella Á Testosterone Á Aggression Á in response to social challenge, but were aggressive and Latitude Á Androgen spent more time within 5 m of a decoy during a simulated territorial intrusion (STI) than early breeding males. Male Introduction Communicated by C. G. Guglielmo. Numerous studies have described aggressive territoriality and the regulation of androgen secretion in breeding male passe- D. W. Wacker Graduate Program in Neurobiology and Behavior, rines (Harding and Follett 1979;Huntetal.1995; Meddle et al. University of Washington, Box 351800, Seattle, 2002; Wingfield 1984, 1985; Wingfield and Hahn 1994). WA 98195, USA Many have utilized models from the family Emberizidae,most notably the White-crowned Sparrow, Zonotrichia leucophrys, D. W. Wacker (&) Centre for Integrative Physiology, and Song Sparrow, Melospiza melodia. Aggression in University of Edinburgh, Edinburgh EH8 9XD, UK Emberizids is usually high in the early breeding season during e-mail: [email protected] territory initiation and is associated with elevated circulating androgen levels. These levels typically decrease in the mid– A. J. Coverdill Á C. M. Bauer Department of Biology, University of Washington, late breeding season, but are still elevated when compared Box 351800, Seattle, WA 98195, USA with levels in non-breeding life history stages (Hunt et al. 1999; Wingfield and Farner 1978;WingfieldandHahn1994). J. C. Wingfield Males in pairs that normally produce multiple broods College of Biological Sciences, University of California Davis, BRIGGS 294, within a single breeding season, such as the Puget Sound Davis, CA 95616, USA subspecies of the White-crowned Sparrow, Zonotrichia 123 80 J Ornithol (2010) 151:79–86 leucophrys pugetensis, often respond to conspecific territo- et al. 2007). Therefore, high latitude breeding males that rial challenges in the mid–late breeding season by tran- provide paternal care in pairs that produce single broods siently increasing plasma androgens (Wingfield et al. 1990, should have high androgen levels in the early breeding 2007; Wingfield and Hahn 1994). This is hypothesized to season as compared to the mid–late breeding season and allow these males to reap the benefits of having high should not up-regulate androgen secretion in response to androgen levels during a territorial dispute without suffering social challenge in later breeding substages. the energetic costs associated with maintaining these levels Subspecies comparisons within Zonotrichia leucophrys continually (Wingfield et al. 1990, 2001). Males in species have presented an excellent model for investigating the or populations that typically do not raise multiple broods, latitudinal regulation of androgen secretion, its social such as the high arctic breeding Gambel’s White-crowned modulation, and how it affects aggressive breeding territo- Sparrow, Zonotrichia leucophrys gambelii, and Lapland riality. However, in order to generalize these findings, it is Longspur, Calcarius lapponicus, do not transiently up-reg- necessary to establish an additional model passerine, and ulate circulating androgens during territorial disputes especially Emberizid species and subspecies, to investigate (Goymann et al. 2007; Hunt et al. 1995; Meddle et al. 2002). these phenomena and tease apart the possible effects of The breeding season for high latitude breeding birds is phylogeny (Hirschenhauser et al. 2003). The Fox Sparrow, both short and synchronous, as dictated by the brevity of Passerella iliaca, has potential in this regard. While there is the arctic summer (Hunt et al. 1995; Wingfield and Hunt currently only one recognized species of Fox Sparrow, 2002). Owing to this synchronicity, many arctic breeding Passerella iliaca (A.O.U. 1998), there has been ongoing birds are obligatorily singly brooded, and it is therefore scholarly discussion regarding separation of this taxon into uncommon for one male to be in an early territory initiation four separate species, the Red Fox Sparrow (Passerella phase while another neighboring male is in a later breeding iliaca), Sooty Fox Sparrow (Passerella unalaschcensis), substage in these regions, especially in monogamous spe- Slate-colored Fox Sparrow (Passerella schistacea), and cies where males provide some paternal care (Hunt et al. Thick-billed Fox Sparrow (Passerella megarhyncha) (Burns 1995; Wingfield et al. 1990). Interestingly, peak testoster- 1993; Weckstein et al. 2002; Zink 1994; Zink and McKitrick one levels are positively correlated with absolute latitude 1995; Zink and Weckstein 2003). Currently, these potential (Garamszegi et al. 2008). These levels reflect early species are referred to simply as ‘‘groups’’. Within these four breeding when sexual behavior is displayed and territories groups are 14–18 subspecies whose distributions span areas are initiated (Garamszegi et al. 2008; Hunt et al. 1995; of the western United States and much of Canada (A.O.U. Wingfield et al. 1990). Birds that migrate long distances to 1957; Cramps and Perrins 1994; Weckstein et al. 2002). breed over a short season are hypothesized to encounter Within these subspecies, there are long- and short-distant high levels of conspecific competition for mates and ter- migrants (Austin 1968; Bell 1997; Mailliard 1921), altitu- ritories upon arrival on their breeding grounds, thus they dinal migrants (Swarth 1920), resident populations (Cramps have higher androgen levels to deal with these conditions and Perrins 1994), and hybridization between groups (Garamszegi et al. 2008; Wingfield et al. 1990). However, (Webster 1975; Zink 1994), making Passerella iliaca ripe high circulating androgen levels in mid–late breeding for subspecies and latitudinal comparisons of aggression and stages would be problematic for species that provide related androgen secretion. Previously, aggressive territo- paternal care, as experimental increases in testosterone riality in Fox Sparrows has received very little scholarly have been shown to negatively affect chick feeding rates attention (Weckstein et al. 2002), but has been observed in and development (Hegner and Wingfield 1987; Hunt et al. free-living males (Blacquiere 1979; Martin 1980). Related 1999; Ketterson et al. 1992; Lynn et al. 2005). Therefore, androgen modulation has yet to be investigated. This paper the ability to socially up-regulate androgen secretion later outlines patterns of male breeding aggression and androgen in the breeding season, to properly respond to territorial secretion at multiple latitudes in the Fox Sparrow. We have disputes and/or prepare for mating to produce subsequent examined two subspecies within two groups of migratory broods, uncommon at these latitudes, may have been lost. Fox Sparrow, the Red Fox Sparrow, P. i. zaboria, and the Male passerines that only show aggression for brief periods Sooty Fox Sparrow, P. i. sinuosa. at the beginning of their breeding season and provide high levels of parental care are more likely