The Auk 120(3):591–599, 2003

OVERVIEW TREE (TACHYCINETA BICOLOR): A NEW MODEL ORGANISM?

JASON JONES1 Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire, 03755, USA

THE TREE (Tachycineta bicolor) has WHAT HAVE WE LEARNED FROM THE been the focus of a diversity of research that is ? rivaled by few other . A quick search through the Science Citation Index reveals over Tree Swallow research has covered a highly 400 manuscripts either focusing on or involving diverse array of subjects including extrapair Tree Swallows in the last 25 years, on topics paternity (Lifjeld and Robertson 1992, Lifjeld et ranging from mating systems to nest-building al. 1993), infanticide (Robertson 1990), delayed behavior, from climate change to environmental plumage maturation in females (Stutchbury contamination. Here, I focus on two themes: (1) and Robertson 1987a), costs of reproduction the Tree Swallow as a “new” model organism, (Wheelwright et al. 1991), senescence (Robertson and (2) Tree Swallow research fi ndings that and Rendell 2001), climate change (Dunn and have important implications for all avian biol- Winkler 1999), and pollution (McCarty and ogy and, indeed, biology in general. Secord 1999a, b), to name just a few. Given this breadth, I could not hope to do it all justice in THE TREE SWALLOW AS A “NEW” MODEL ORGANISM this article. As a consequence, I have selected two areas of Tree Swallow research that I feel To appreciate the diversity of research un- have had an important infl uence on avian dertaken with Tree Swallows, we must fi rst biology—mating systems and reproductive understand why so many researchers use Tree behavior, spatial relationships and individual Swallows as their focal organism. Model organ- movements; and two areas whose infl uence is isms tend to have four features in common: just beginning to be felt—timing of life-history rapid development and short generation time, events relative to climate change, indicators of small adult size, ready availability, and tracta- environmental contamination. bility (Bolker 1995). Whereas the Tree Swallow falls a little short on the fi rst two compared to MATING SYSTEMS AND REPRODUCTIVE BEHAVIOR traditional model organisms, the fact that this species readily breeds in nest boxes makes it Extrapair paternity and mate choice.—Extrapair about as available and tractable a study organ- paternity is now widely recognized as a fre- ism as any avian biologist could hope for. That quently occurring phenomenon among socially feature allows researchers to set population monogamous (e.g. Griffi th et al. 2002). The sizes, control external perturbations (e.g. pre- extent of extrapair paternity in a population dation), as well as standardize and manipulate depends on interactions among three individu- nest-site characteristics and contents (e.g. cavity als: the extrapair male and his ability to obtain volume, brood manipulations). In addition, the extrapair copulations, the social male and his ease with which individuals can be captured ability to protect paternity in his nest, and the and uniquely marked greatly facilitates re- female and her proclivity for seeking extrapair search activities. All those factors combine to copulations (Westneat et al. 1990, Dunn et al. allow researchers fl exibility unavailable with 1994a). Extrapair paternity appears to be more most other bird species. In fact, I would argue common in Tree Swallows than in most other that Tree Swallows deserve equal standing be- species; 50–90% (Dunn et al. 1994a) compared side fruit fl ies, nematodes, and mice as one of to an average of 14% for other species (Birkhead the classical model organisms in biology. and Møller 1992), a high frequency that is not an artifact of nest boxes (Barber et al. 1996). In ad-

1 dition, the prevalence of extrapair paternity also E-mail: [email protected] varies widely between years within a breeding 591 592 Overview [Auk, Vol. 120 population (e.g. 50% of broods in one year, territory. For females, that could take the form 87% the next) and between individuals within of intraspecifi c brood parasitism (Gowaty 1985, a single population (Dunn et al. 1994a). Those Sandell and Diemer 1999); for males, extrapair factors, when combined with the ability to cap- paternity (Petrie and Kempenaers 1998). ture and sample complete family groups, have Tree Swallows, as secondary cavity nesters, allowed Tree Swallow researchers a unique op- are often strongly nest-site limited (Holroyd portunity to examine the relative strengths of 1975). As a consequence, there are always in- the three players in the extrapair mating game. dividuals of both sexes who are unable obtain Perhaps the most interesting fi nding of Tree to nest sites or mates or both. Female Tree Swallow extrapair research is that extrapair Swallows do not reproduce until they can copulations are almost completely under the obtain a nest site (Stutchbury and Robertson control of the female (Venier and Robertson 1987b); intraspecifi c brood parasitism is very 1991, Lifjeld and Robertson 1992, Venier et al. uncommon in this species (Lombardo 1988, 1993, Dunn et al. 1994b). In fact, female prefer- Barber et al. 1996, Kempenaers et al. 1999). ence appears to override most other factors that Most female fl oaters are one-year-old females have the potential to infl uence the opportunity (Stutchbury and Robertson 1987b) who do not for extrapair activity (e.g. nest-box location, breed although they do spend a considerable nest-box density, breeding synchrony, experi- amount of time prospecting for nest sites. ence; Dunn et al. 1994b). However, there are no The Tree Swallow is one of only two species consistent across-year patterns with respect to in North America in which only the female and the characteristics of males selected by females not the male displays delayed plumage matura- (e.g. size, experience, arrival date) that allow the tion (Hussell 1983, Stutchbury and Robertson clear defi nition of a high-quality mate (Dunn et 1987a; the other is the Hooded Warbler [Wilsonia al. 1994a, Barber et al. 1998, Conrad et al. 2001). citrina], Morton 1989). Subadult Tree Swallow Indeed, one could conclude from those studies females have a dull brownish plumage that that the defi nition of a high-quality mate is not a contrasts strongly with iridescent blue plum- fi xed defi nition; rather, it may change both with age of adult males and females (Hussell 1983). and among breeding seasons as ambient condi- Stutchbury and Robertson (1987a) hypoth- tions change (e.g. weather, food availability, esized that the distinctive plumage of subadult talent pool). females served to reduce aggression by resident Importance and role of fl oaters.—Whenever males (sexual signaling) and resident female breeding resources are limited, there is a poten- (subordinate signaling), thereby facilitating ex- tial for a proportion of a population to be unable ploration. Resident males tended to be less ag- to breed despite being reproductively mature gressive to subadult females than to intruding (e.g. Brown 1969, Smith 1978). In some species, adult females, whereas resident females were such as the Tree Swallow, that proportion can equally aggressive towards subadult and adult be quite large (Stutchbury and Robertson 1985). intruders. Those results and others (Lozano and As a consequence, understanding the role of Handford 1995) imply that female subadult fl oaters can be an important component of un- plumage is primarily an intersexual signaling derstanding a species’ population dynamics. adaptation. There are at least three theories concerning the Unlike female fl oaters, however, male fl oaters characteristics of fl oating individuals. The fi rst are able to obtain a modest degree of reproduc- theory contends that fl oating individuals are tive success despite not defending a nest box. younger or competitively inferior individuals or In one study (Kempenaers et al. 2001), fl oaters both who were unable to obtain a breeding op- were responsible for 13% of extrapair young to portunity (e.g. Shutler and Weatherhead 1992). which the researchers could assign paternity. The second theory contends that individuals Again unlike females, there were few differ- choose to forego breeding in the hope of obtain- ences—morphological or otherwise—between ing a high-quality nest site or territory should fl oater and resident males, other than a ten- one come available (e.g. Zack and Stutchbury dency for males who participated in extrapair 1992). The third theory contends that fl oating matings (including fl oaters) to be heavier than is a viable alternative reproductive strategy to those that did not. That study supported previ- holding and defending a nest-site or breeding ous observations that male fl oaters participate July 2003] Overview 593 in extrapair copulations (Barber and Robertson confi dence, male parental care, and offspring re- 1999), but was one of the fi rst to document suc- cruitment. In species such as the Tree Swallow, cessful reproduction by fl oaters in any passer- where male care positively affects offspring ine species (see Ewen et al. 1999). recruitment (Leffelaar and Robertson 1986), one Mate guarding, paternity confi dence, paternal would predict a positive relationship between care, and infanticide.—Ever since researchers con- paternity confi dence and male parental care; the fi rmed the existence of extrapair mating strate- shape of the curve depends on the strength of gies in birds, there has been an interest in (1) the relationships between care and recruitment. whether or not males can prevent females from In Tree Swallows, empirical evidence indicates engaging in extrapair activity and vice versa, that paternity confi dence appears to have little and (2) whether or not males can tell if there effect on male parental care unless the prob- are extrapair young in their own nests. Male ability of paternity is very low (Robertson 1990, birds employ several behaviors in an attempt to Whittingham et al. 1993); that matches fi ndings minimize the extrapair activity undertaken by for other socially monogamous species (e.g. their social mate. First, they can attempt to pre- Indigo Bunting [Passerina cyanea]; Westneat vent the settlement of conspecifi c pairs nearby 1988). There are at least two reasons for that lack (Rendell and Robertson 1994). Second, they can of a relationship. One is that males are unable to maintain visual vigilance over their social mate assess the proportion or likelihood of extrapair and interrupt any extrapair activity (Birkhead young in their nests, except in extreme cases. If 1979). Third, males may attempt to copulate that is the case, then it behooves males to contin- with their social mate as frequently as possible ue caring for nestlings on the chance that some to win the sperm competition battle (Birkhead of them are theirs. Alternatively, males may feel et al. 1989). Research into those behaviors in “confi dent” in their guarding behaviors such Tree Swallows has led to the conclusion that that they have no need to question the paternity male behavior is largely dictated by female ac- of their brood. Females may bolster that confi - tivity (Chek and Robertson 1994, Whittingham dence by soliciting and accepting copulations et al. 1994). Given that female Tree Swallows from their social mates after absences from the appear determined to participate in extrapair nest site (Kempenaers et al. 1998). activity, frequent copulation may be a more Another alternative avenue to examine a effi cient strategy to insure paternity than is male’s ability to assess paternity is to perform intense following (Venier and Robertson 1991, a removal experiment (i.e. remove the resident Whittingham et al. 1994); it is less energetically male) and monitor the behavior of the replace- costly and provides the male opportunities to ment male. Removal experiments with Tree pursue his own extrapair activities. However, Swallows have led to some interesting and given the prevalence of extrapair young in Tree startling results concerning the lengths that Swallow nests (Lifjeld et al. 1993), it appears that males will go to insure paternity (Robertson whatever strategy males adopt are not particu- and Stutchbury 1988, Robertson 1990). If a larly effective. Indeed, mate guarding (either by male is removed during the egg-laying stage, following or frequent copulation) may only be the replacement male tends to adopt the brood, a viable paternity confi dence strategy when fe- because there is a probability that he has at least males have little interest in pursuing extrapair partial paternity (Roberston 1990). Replacement activities (Chek and Robertson 1994). males that arrive after clutch completion but How males ascertain the presence of extra- early in incubation tend to adopt the brood pair young in their nests is unclear. Because it whereas males that arrive late in incubation is diffi cult to test nestling recognition by males tend to commit infanticide, killing the nestlings directly in the fi eld, we need to identify behav- after they hatch to induce the female to renest. iors that are proxies for paternity confi dence. Similarly, replacement males that arrive dur- One obvious candidate is male parental care. ing the nestling stage almost always commit Building on parental-investment theory which infanticide (Robertson and Stutchbury 1988, predicts a decrease in male parental care with a Robertson 1990). Infanticide in Tree Swallows decrease in paternity confi dence (Trivers 1972), appears to be a sexually selected behavior. Whittingham et al. (1992) outlined a theoretical Unmated males that are infanticidal are able to framework for the trade-offs among paternity obtain a breeding opportunity and, hence, will 594 Overview [Auk, Vol. 120 have a higher potential fi tness than unmated opportunity for extrapair activity (Rendell and males that are not infanticidal (Robertson and Robertson 1994). In addition, females may de- Stutchbury 1988, Robertson 1990). fend extra nest sites to facilitate re-nesting in the Females are not passive by-standers in that event of a nest failure. Those results provide in- somewhat macabre scenario. Females tend teresting insights into the potentially confl icting to be receptive to replacement males during motivations behind male and female territorial- egg-laying and incubation and may attempt to ity and resource defense. pacify the replacement males by readily accept- So, what about after the breeding season? ing copulations (Robertson 1991). However, The decision whether or not to disperse, for when the replacement male arrives during the both adults and juveniles, is ultimately based nestling stage, females react very aggressively on a cost–benefi t analysis. By dispersing, an to their presence and may, in some cases, be individual is entering an unknown area, giving able to prevent infanticide (Robertson 1991). up information on resource availability, preda- Interestingly, female Tree Swallows are also tor abundance, and possibly mating opportuni- known to commit sexually selected infanticide, ties. On the other hand, a dispersing individual likely driven by nest-site limitation (Shelley may fi nd abundant resources and better mates 1934, Robertson and Stutchbury 1988, Chek and (Clobert et al. 2001). For adult birds, it has Robertson 1991). Chek and Robertson (1991) been hypothesized that a poor breeding season removed four females during incubation and should motivate individuals to fi nd greener pas- four during the nestling stage. All the incuba- tures (Greenwood and Harvey 1982). However, tion replacements buried the existing eggs with empirical evidence suggests that is not always a new nest and laid their own clutch. Only two the case (e.g. Lindberg and Sedinger 1997), al- of the four experimental nestling-removal boxes though the reasons for that are unclear. Even received a replacement female. One of those fe- less clear are patterns and motivators behind males ignored the nestlings until they died; the natal dispersal (but see Brown 1987). dead nestlings disappeared from the nest box Tree Swallows provide a perhaps unique and she started her own clutch. The second re- opportunity to examine both adult and juve- placement female committed infanticide. nile dispersal. Individuals are easily captured and marked which facilitates measurements SPATIAL RELATIONSHIPS AND INDIVIDUAL MOVEMENTS of internest movements and shows reasonably high local and regional site fi delity (reviewed Nest-site competition drives a large propor- in Robertson et al. 1992), thereby improving tion of Tree Swallow reproductive behavior. It sample sizes for analytical purposes. Shutler also shapes the spatial relationships exhibited and Clark (2003) took advantage of those fac- by nesting birds and dispersing individuals. tors in their long-term study (12 years) of adult Nesting Tree Swallows exhibit a distinct con- and natal dispersal in Tree Swallows. They cept of personal space. In both natural cavities tested three sets of relationships: between and nest-box grids, nesting pairs attempt to nest breeding success and adult dispersal; among as far from other pairs as possible (Robertson manipulated clutch size, adult dispersal, and and Rendell 1990) and will attempt to prevent natal dispersal; and between breeding suc- conspecifi cs from nesting in close proximity cess and dispersal distance. Contrary to their (Muldal et al. 1985, Lombardo 1987), often by predictions, however, neither adult nor natal concurrently defending two or more nest sites dispersal distances were related to breeding (Harris 1979, Robertson and Gibbs 1982, Rendell success, nor did manipulating breeding suc- and Robertson 1989). The benefi ts of extranest cess affect dispersal. Furthermore, dispersal defense are likely sex-specifi c. For males, de- distance had no signifi cant effect on breeding fending extra sites may increase the probability success the following year. Shutler and Clark of attracting a second mate (resource defense (2003) hypothesize that because, in most years, polygyny, Dunn and Hannon 1991, Rendell and most nests produced at least some breeding Robertson 1994). Resident females, on the other success (i.e. at least one fl edgling) and because hand, may defend extra sites to achieve the individual nest sites did not consistently pro- opposite result, namely to prevent settlement duce high breeding success, individuals would of other females, thereby minimizing a male’s have little to gain by moving to a new site. In July 2003] Overview 595 addition, because individuals appear to be be best appreciated as a regional, rather than highly box-faithful between years (Robertson continental, phenomenon. That fi nding has im- et al. 1992, Shutler and Clark 2003), the infl u- portant implications for the examination of the ence of social interactions on site fi delity and effects on birds of other widespread phenom- dispersal cannot be discounted. ena (e.g. El Niño Southern Oscillation, hemlock woolly adelgid [Adelges tsugae] outbreaks). TIMING OF LIFE HISTORY EVENTS RELATIVE TO CLIMATE ENVIRONMENTAL CONTAMINATION

There is a growing body of evidence detail- The detrimental effects of environmental ing ecological effects of global warming on the contaminants created as a by-product of hu- earth’s biota (e.g. Ottersen et al. 2001). Trends man activity have long concerned scientists uncovered in the bird world include the ad- and environmentalists. Partly due to their vancement of egg-laying (Crick et al. 1999), de- charismatic nature, birds and the negative ef- synchronization of onset of breeding and food fects of contaminants on them have been the abundance (Visser et al. 1998), and alteration focus of ecotoxicology research for many years. of population growth rates (Sæther et al. 2000). For example, population declines of birds were However, most of that bird research has been the fi rst indicators of environmental contamina- undertaken in Europe and long-term or large- tion by lead (Grinnell 1894), pesticides (Carson scale studies are rare in North America (for 1962), and polychlorinated biphenyls (PCBs; notable exceptions see Brown et al. 1999 and Jensen et al. 1969). Nott et al. 2002). Tree Swallows provide a use- Of environmental contaminants, PCBs are ful model for examining large-scale phenom- among the most widespread and well studied. ena in North America (see Winkler et al. 2002), One area of specifi c interest is the magnitude given their continent-wide range and the ease and regularity of transfer of PCBs from sites with which breeding activity can be monitored. of deposition in aquatic systems into terrestrial Recently, Dunn and Winkler (1999) published ecosystems and food webs. Recent research has an analysis of 3,450 Tree Swallow nest records focused on Tree Swallow behavior and repro- collected over 40 years (1952–1992) across North ductive performance as an index of that uptake America. They uncovered an advancement of and transfer from aquatic to terrestrial systems fi ve to nine days in egg-laying date that they (McCarty and Secord 1999a, b; Golden and associated with increasing air surface tempera- Rattner 2003). tures during the breeding season and, given the Tree Swallows have the potential to be an scope of their sampling, reasonably concluded that this trend toward earlier breeding likely effective indicator species for PCB contamina- encompasses all Tree Swallows breeding in tion: they are abundant and their biology is well North America. understood (Robertson et al. 1992); they nest However, there is some evidence that climate willingly in nest boxes; and they feed largely change may not affect all aspects of a species’ on insects with aquatic larval stages, thereby range in a similar manner (Visser et al. 1998) potentially providing an assay of aquatic con- and that climate patterns themselves also ex- tamination and biomagnifi cation (Bishop et al. hibit signifi cant spatial variation (Easterling et 1995, McCarty and Secord 1999b, Secord et al. al. 2000). With that in mind, Hussell (2003) pre- 1999). Furthermore, there is a large body of sented results of a long-term study (1961–2001) evidence that PCBs accumulate in eggs and of Tree Swallows nesting on and near Long bodies of nestlings and adults (e.g. Custer et Point, Ontario, an area not covered by Dunn al. 2002). However, the ultimate utility of the and Winkler’s (1999) sampling. Hussell’s (2003) Tree Swallow as a bioindicator will depend on results indicate that although spring tempera- the ability of researchers to accurately describe tures were an important predictor of the timing natural variation (i.e. baseline variation) in the of egg laying, there was no evidence for increas- trait they wish to use as the indicator (e.g. popu- ing spring temperatures in the Long Point area. lation size, breeding success) to accurately mea- As a consequence, the effect of changing spring sure a response to a perturbation (Cottingham temperatures on Tree Swallow breeding would and Carpenter 1998). 596 Overview [Auk, Vol. 120

CONCLUSION BROWN, J. L. 1969. Territorial behavior and popu- lation regulation in birds. Wilson Bulletin 81: As I began my graduate career, I recall regu- 293–329. larly chiding my dissertation supervisor about BROWN, J. L. 1987. Helping and Communal Breeding in Birds: Ecology and Evolution. his choice of study organism. How could you Princeton University Press, Princeton, New possibly fi nd satisfaction studying a box-nester? Jersey. Where is the challenge in studying the avian BROWN, J. L., S.-H. LI, AND N. BHAGABATI. 1999. equivalent of a white rat? Well, as I struggled Long-term trend toward earlier breeding in through my studies and the small samples sizes an American bird: A response to global warm- and ecological noise created by my own choice ing? Proceedings of the National Academy of of a model organism, I learned a valuable lesson Science USA 96:5565–5569. about being seduced by the appeal or attractive- CARSON, R. 1962. Silent Spring. Houghton Mifflin, Boston, Massachusetts. ness of a study organism. The Tree Swallow CHEK, A. A., AND R. J. ROBERTSON. 1991. Infanticide may not be the most glamorous model organ- in female Tree Swallows: A role for sexual se- ism, but it has certainly proven to be one of the lection. Condor 93:454–457. most productive in avian biology. CHEK, A. A., AND R. J. ROBERTSON. 1994. Weak mate guarding in Tree Swallows: Ecological con- ACKNOWLEDGMENTS straint or female control? Ethology 98:1–13. CLOBERT, J., E. DANCHIN, A. A. DHONDT, AND J. Thanks to R. J. Robertson for reviewing the manu- D. NICHOLS, EDS. 2001. Dispersal. Oxford script and for putting up with my chiding. University Press, Oxford. CONRAD, K. F., P. V. JOHNSTON, C. CROSSMAN, B. KEMPENAERS, R. J. ROBERTSON, N. T. WHEELWRIGHT, LITERATURE CITED AND P. T. BOAG. 2001. High levels of extra-pair paternity in an isolated, low-density, island BARBER, C., AND R. J. ROBERTSON. 1999. Floater males population of Tree Swallows (Tachycineta bi- engage in extrapair copulations with resident color). Molecular Ecology 10:1301–1308. female Tree Swallows. Auk 116:264–269. COTTINGHAM, K. L., AND S. R. CARPENTER. 1998. BARBER, C., R. J. ROBERTSON, AND P. T. BOAG. 1996. Population, community, and ecosystem vari- The high frequency of extra-pair paternity in ates as ecological indicators: Phytoplankton re- Tree Swallows is not an artifact of nestboxes. sponses to whole-lake enrichment. Ecological Behavioral Ecology and Sociobiology 38: Applications 8:508–530. 425–430. CRICK, H. Q. P., AND T. H. SPARKS. 1999. Climate BARBER, C., R. J. ROBERTSON, AND P. T. BOAG. 1998. change related to egg-laying trends. Nature Experimental mate replacement does not in- 399:423–424. crease extra-pair paternity in Tree Swallows. CUSTER, T. W., C. M. CUSTER, AND R. K. HINES. 2002. Proceeding of the Royal Society of London, Dioxins and congener-specifi c polychlorinated Series B 265:2187–2190. biphenyls in three avian species from the BIRKHEAD, T. R. 1979. Mate guarding in the Magpie, Wisconsin River, Wisconsin. Environmental Pica pica. Behaviour 27:866–874. Pollution 119:323–332. BIRKHEAD, T. R., F. M. HUNTER, AND J. E. PELLATT. DUNN, P. O., AND S. J. HANNON. 1991. Intraspecific 1989. Sperm competition in the Zebra Finch, competition and the maintenance of monog- Taeniopygia guttata. Animal Behaviour 38: amy in Tree Swallows. Behavioral Ecology 2: 935–950. 258–266. BIRKHEAD, T. R., AND A. P. MØLLER 1992. Sperm DUNN, P. O., R. J. ROBERTSON, D. MICHAUD-FREEMAN, Competition in Birds: Evolutionary Causes AND P. T. BOAG. 1994a. Extra-pair paternity in and Consequences. Academic Press, London. Tree Swallows: Why do females mate with BISHOP, C. A., M. D. KOSTER, A. A. CHEK, D. J. more than one male? Behavioral Ecology and T. HUSSELL, AND K. JOCK. 1995. Chlorinated Sociobiology 35:273–281. hydrocarbons and mercury in sediments, DUNN, P. O., L. A. WHITTINGHAM, J. T. LIFJELD, R. Red-winged Blackbirds (Agelaius phoenicus) J. ROBERTSON, AND P. T. BOAG. 1994b. Effects and Tree Swallows (Tachycineta bicolor) from of breeding density, synchrony, and experi- wetlands in the Great Lakes-St. Lawrence ence on extrapair paternity in Tree Swallows. River basin. Environmental Toxicology and Behavioral Ecology 5:123–129. Chemistry 14:491–501. DUNN, P. O., AND D. W. WINKLER. 1999. Climate BOLKER, J. A. 1995. Model systems in developmen- change has affected the breeding date of tal biology. BioEssays 17:451–455. Tree Swallows throughout North America. July 2003] Overview 597

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