A Long-term Study of Western Bluebirds
Studies of western bluebirds (Sialia mexicana) began with placement of 363 nest boxes placed on Hastings Reserve and the adjacent Oak Ridge Ranch in 1983-1985. This long-term study, led by Prof. Janis Dickinson (Cornell University) has focused primarily on the evolution of social behavior, including mating systems, parental care, and cooperative breeding (Dickinson et al. 2016).
The Research
The theoretical underpinnings of this research are derived from ideas proposed by Charles Darwin, W.D. Hamilton, and R.L. Trivers. The synthesis of these ideas is that behavioral traits evolve because they increase the ability of individuals to propagate copies of their genes, either by increasing the number and quality of offspring they, themselves, produce or by enhancing the number and quality of offspring produced by relatives (via kin selection). This body of theory predicts both cooperation and conflict within individuals, families, within and between the sexes, and within animal societies. Much of the research on western bluebirds to date has focused on the nature of these cooperative and competitive behaviors, the diversity of behavioral and morphological adaptations they produce, and the tradeoffs they involve. By combining long-term research of marked individuals with molecular genotyping much has been learned about how these fitness tradeoffs shape the behavioral choices animals make throughout their lives.
This body of theory predicts both cooperation and conflict within individuals, families, within and between the sexes, and within animal societies.
One of the main questions we have addressed over the years has been why western bluebird sons stay at home during their first winter (while most daughters tend to disperse) and why they sometimes help at the nests of their parents or brothers. Western bluebirds live in family groups, often with retained sons and immigrant females that dispersed into the group in late summer (Kraiijeveld & Dickinson 2001). The sons then tend to settle nearby to breed with females that joined their winter group. It turns out – after quantifying mistletoe on 3,377 oak trees – that the fruit made available by mistletoe lasts all winter and is an important driver of this delayed and localized dispersal of sons. When we removed half the mistletoe from 13 territories, nearly all sons left, whereas their parents stayed; in contrast, most sons on control territories remained at home with their parents (Dickinson & McGowan 2005). Further investigation indicated that both the presence of parents and mistletoe volume are important to whether or not sons stay at home (Dickinson et al. 2014). Mothers are less aggressive to their sons and daughters than to same aged immigrant birds that occasionally join their winter groups (Dickinson et al. 2009). This nepotism allows sons and daughters greater access to food. Overwinter survival of sons in these winter groups is the highest reported for any bird species – 95% of first-winter males living in winter groups survive until spring!
After winter, sons tend to bud off a portion of their parents’ territory to breed on their own and most of the mistletoe they acquire on their own territory comes from their parents (Dickinson et al. 2014). Even so, the parents are somewhat selfish, because the area they concede to their sons has a lower density of mistletoe than does the area they keep from themselves! While parents and sons have separate territories in spring, they share a bit more space than parents will share with unrelated neighbors. The social system is very fluid. Some sons (those that don’t get a mate) stay home and help, other sons come home to help if they lose their mate – no matter what their age, and some sons move back and forth across territories to help at their parents’ nest and feed at their own nest within a single day (Dickinson & Akre 1998). When sons stay home to help, their parents fledge more young, however, the genetic benefit they get from this (through enhancing propagation of genetic material identical to that which they inherited from their parents) is much smaller than the fitness of breeding on their own, leading to the conclusion that it is always better for sons to breed (Dickinson 1996; Dickinson & Akre 1998). A shortage of females in the adult population explains why sons adopt the inferior option of becoming a nonbreeding helper (Dickinson 2001).
The other major focus of the project has been sexual selection and parental care. Although pairs usually mate for life, western bluebird females often mate outside their pairbond so that 45% of females have at least some nestlings that are not sired by their social mate, the caregiving male (Dickinson & Akre 1998). When extrapair males come onto the territory of the pair, they are chased by the resident male, who begins guarding his mate, mostly by following her closely, about 10 days before laying (Dickinson & Leonard 1996; Dickinson 1997). When extrapair males try to copulate with females, the females are very good at thwarting these attempts, but if the male is older, and especially if he is older than their mate, females tend to be more receptive to these copulation attempts (Dickinson 2001). Use of molecular markers showed that older males tend to sire most of the extrapair young and when they do, they don’t lose any more paternity in their own nests than do males that do not sire extrapair young (Ferree & Dickinson 2011, 2014). As such, these older males that are successful extrapair sires have double the reproductive success of males that don’t have extrapair young (Ferree & Dickinson 2014). Amber Budden (2009), a another former postdoc on the project, showed that older males have brighter plumage than younger males, which may be one way that females discriminate older males.
The bluebird project is ideal for involving students and postdocs in research, because the population is always ripe for new questions that can benefit from a combination of novel experimental studies, use of molecular techniques, and access to long-term data on survival and reproduction. Andy McGowan collaborated on the mistletoe studies. Amber Budden worked on plumage coloration. Elise Ferree, postdoctoral associate, studied the genetic and fitness consequences of extrapair mating and extrapair paternity. Caitlin Stern, a former Ph.D. student in Neurobiology and Behavior at Cornell, showed that benefits of delayed dispersal (where sons stay home with their parents) include cryptic, helpful interactions among male relatives living in kin neighborhoods – wherein males come to the aid of nearby relatives if they hear a scream or if an intruder is placed on the territory. Çağlar Akçay, postdoctoral associate, studied social cognition – showing western bluebirds use vocalizations to tell which individuals are relatives and how old their neighbors are. Over the years, the western bluebird project has been a training ground for undergraduates and recent post-graduate interns without whose efforts the project could not have been successful; more than 80% of our >100 interns have gone on to graduate school. Several now hold professorships and lectureships at colleges or universities.
LITERATURE CITED
Akcay, C., Swift, R.J., Reed, V.A., and J.L. Dickinson. 2013. Vocal kin recognition in kin neighborhoods of western bluebirds. Behavioral Ecology 24: 898-905. doi: 10.1093/beheco/art018
Budden, A.E. and J.L. Dickinson. 2009. Signals of quality and age: the information content of multiple plumage ornaments in male western bluebirds, Sialia mexicana. Journal of Avian Biology 40:18-27.
Dickinson, J.L. 1997. Male detention affects extra-pair copulation frequency and pair behaviour in western bluebirds. Animal Behaviour 53: 561-571.
Dickinson, J.L. 2001. Extrapair copulations in western bluebirds: female receptivity depends on male age. Behavioral Ecology and Sociobiology 50: 423-429.
Dickinson, J.L. 2004. Facultative sex ratio adjustment by western bluebird mothers with stay-at-home helpers-at-the-nest. Animal Behaviour 68: 373-380.
Dickinson, J.L., M. Euaparadorn, K. Greenwald, C. Mitra, D. Shizuka. 2009. Cooperation and competition: nepotistic tolerance and intra-sexual aggression in western bluebird winter groups. Animal Behaviour 77: 867-872.
Dickinson, J.L., Akçay, C., Ferree, E.D., and C.A. Stern. 2016a. Western bluebirds: lessons from a marginal cooperative breeder. In Koenig, W.D. and J.L. Dickinson (eds), Cooperative breeding in vertebrates: Studies of Ecology, Evolution, and Behavior. Cambridge, UK: Cambridge University Press.
Dickinson, J.L. and J.J. Akre. 1998. Extrapair paternity, annual inclusive fitness, and within-group benefits of helping in the western bluebird. Molecular Ecology 7: 95-105.
Dickinson, J.L., Ferree, E., Stern, C.A., Swift R., and B. Zuckerberg. 2014. Delayed dispersal in western bluebirds: Teasing apart the importance of resources and parents. Behavioral Ecology, 25: 843-851.
Dickinson, J.L. and M.L. Leonard. 1996. Mate attendance and copulatory behaviour in western bluebirds: evidence of mate guarding. Animal Behaviour 52: 981-992.
Dickinson, J.L., W.D. Koenig, and F.A. Pitelka. 1996. The fitness consequences of helping behavior in the western bluebird. Behavioral Ecology 7: 168-177.
Dickinson, J.L. and A. McGowan. 2005. Resource wealth drives family group living in western bluebirds. Proceedings of the Royal Society, London B 272: 2423 – 2428.
Ferree, E.D. and J.L. Dickinson. 2011. Natural extra-pair paternity matches receptivity patterns in unguarded females: Evidence for importance of female choice. Animal Behaviour 83: 1167-1173 [Editor’s Choice].
Ferree, E.D. and J.L. Dickinson. 2014. Male western bluebirds that sire extra-pair young are also successful within-pair mates. Animal Behaviour 90: 11-19.
Kraaijeveld, K. and J.L. Dickinson. 2001. Family-based winter territoriality in western bluebirds: the structure and dynamics of winter groups. Animal Behaviour. 61: 109-117.
Stern CA. 2012. Cooperation and competition in kin associations. Neurobiology and Behavior. Ithaca: Cornell University.