Translator Disclaimer
1 April 2005 CAN BREEDING HABITAT BE SEXUALLY SELECTED?
Author Affiliations +

I propose that sexual dynamics, through mechanisms of sexual selection, can in part determine what constitutes specific breeding habitat. In this view, breeding-habitat features chosen by organisms, like certain morphological or other behavioral traits they exhibit, can be sexually selected, with the consequence that breeding habitats may not be uniquely aligned for ecological niche requirements. I distinguish sexual selection from natural selection because I mean to contrast sexual natural selection (sexual selection) from nonsexual natural selection (ecological selection). Thus, I suggest that ecological selection, acting on traits related to physical resources, and sexual selection, acting on traits related to mate choice, are potentially conflicting forces acting on breeding-habitat specificity.

It is hardly novel to contend that sexual relations influence spatial patterns, but those influences have always been believed to operate within the confines of habitat sculpted by ecological selection. Here, sexual selection defines, in part, what constitutes breeding habitat.

Certain predictions arise if sexual selection generates breeding-habitat specificity. Breeding habitat must be specific, though regional differences, including dramatic ones, are consistent with the idea. A shift in, or relaxation of, such specificity in nonbreeding situations is expected, given the flexibility in exploiting resources. Generalized traits, such as beaks equipped to exploit a variety of food sources, are predicted to prevail, because adaptive constraints from one period may compromise adaptive solutions for another. Finally, we would expect social factors to influence habitat occupancy patterns, with spatial clustering, independent of ecological factors, likely. Although none of the foregoing is independent direct evidence that breeding-habitat specificity is a sexual trait mediated by sexual selection, collectively it supports the concept. I suggest that the idea has general applicability, but I focus primarily on migrant birds as a group, because they are especially suited for its consideration.

Breeding-habitat specificity

Habitat specificity is believed to result from evolution of adaptations ecologically selected for the exploitation of niches found in particular habitats. Ecomorphology literature (e.g. Selander 1966, Leisler 1980, Bairlein 1980, James 1982, Polo and Carrascal 1999) both rests on and supports the premise that the morphologies of birds are suited to the niches and habitats they occupy. As a corollary, the notion that organisms should settle in habitats of high intrinsic quality is pervasive (Fretwell and Lucas 1970, Rosenzweig 1991, Ens et al. 1992, Yosef and Grubb 1994). Brown et al. (1995) argued that “hotspot“ concentrations of within-species avian breeding territories, noted by many (e.g. Nice 1937, May 1949, Morse 1989, Jones and Robertson 2001), reflect the extent to which local habitats satisfy the niche requirements of particular species. Certainly, habitat features can be connected to reproductive success (Krebs 1971, Holmes et al. 1996), though fecundity thresholds are met under conditions of excessive food (Tremblay et al. 2003).

Moreover, there is no doubt that birds are habitat-specific, especially during breeding. In a classic paper, MacArthur et al. (1962) began by noting that a competent bird-watcher can “look at a habitat and correctly name the bird species that will breed there in abundance.“ Numerous studies of North American breeding bird communities have found highly nonrandom distributions among plant alliances (Debinski and Brussard 1994, Welsh and Lougheed 1996, King et al. 2000). Paradoxically, that pattern is especially emphasized among those species whose breeding and winter habitats are most dramatically different—Neotropical migrants (Kirk and Hobson 2001).

Breeding-habitat specificity sometimes shows distinct regional variation within species, indicating adaptedness to multiple, though regionally specific, habitats. Hammond’s Flycatcher (Empidonax hammondii), Prairie Warbler (Dendroica discolor), and Swainson’s Warbler (Limnothlypis swainsonii) are examples in which distinctly different habitats are occupied on a regional basis (Nolan 1978, Lambert 1987, Brown and Dickson 1994, Willson and Comet 1996). Flack (1976) reported other instances of habitat switches in birds of the American southwest.

Reduced habitat specificity at other times

Notwithstanding breeding-habitat specificity, most migrant species are capable of successfully occupying very different habitats. Even during breeding, there is evidence that non-breeding habitats are used cryptically for foraging in some species (Lack 1943, Pagen et al. 2000). Other species, when no longer limited by nesting requirements, but prior to autumn departure, broaden the range of habitats exploited (Anders et al. 1998). During migration, birds are less habitat-specific (Wang and Finch 2002), which is not surprising given the variety of environments they pass through and the imperfect information they have access to en route (Shochat et al. 2002). Migrant passerines can be habitat-specific during winter (Murphy et al. 2001), but diverse habitats are frequently occupied during that season (Wunderle and Waite 1993, Latta and Faaborg 2002).

It is arguable that the increased energy demands of reproduction could select for more highly restricted breeding habitat to maximize foraging success. However, molt costs and migration also are energetically demanding, and even in the tropics, studies of foraging (Thiollay 1988, Lovette and Holmes 1995) and stress (Norris et al. 2004) in migrant passerines suggest that energy demands are not easily met during nonreproductive periods. Whether winter conditions are more limiting than breeding conditions, as collective research suggests they may be (Lack 1943, Lozano and Lemon 1998, Confer and Larkin 1999, Katti and Price 1999, Strong and Sherry 2000, Evans et al. 2002, Tremblay et al. 2003; but see Newton 2004 for review), adaptations to breeding conditions are likely to be confounded or at least compromised by prevailing adaptations for nonbreeding situations.

In fact, given the multitude of environments that migrants experience over the course of a year, flexibility in exploiting different habitats is a necessity. Eight of 18 passerines breeding in interior Alaska remain there for approximately three months or less, with a mere 48 days being the average for Alder Flycatchers (E. alnorum) (Benson and Winker 2001). Blackpoll Warblers (D. striata) primarily breed in stunted spruce (Picea sp.) taiga but winter in tropical forests of the western Amazon (Dunn and Garrett 1997). To the extent that such different habitats pose different challenges, adaptive responses must reflect compromises, with a measure of niche-averaging.

Resource exploitation within habitats is also varied

Not only do many species cope well with highly variable environments, empirical studies of migrant species have demonstrated that resource exploitation is highly flexible, arguing for further ecological plasticity. Many studies of guilds of coexisting species have documented overlaps in exploitation of food resources, both in temperate (Wiens 1977, Paszkowski 1984, Holmes 1986, McKnight and Hepp 1998, Rotenberry and Wiens 1998, Ruth and Stanley 2002, Katzner et al. 2003) and in tropical breeding systems (Gotelli et al. 1997, MacNally 2000), especially when food is superabundant (McMartin et al. 2002). Even MacArthur’s (1958) study of spruce-forest-breeding warblers indicated large overlaps in the exploitation of foraging resources by congeneric species. In addition, within-species flexibility in foraging techniques among migrants has been frequently demonstrated (Busby and Sealy 1979, Maurer and Whitmore 1981, Holmes 1994, McCaffery 1998, Chernetsov 2002).

Social factors influence where birds settle

The conventional notion of niche suggests that organisms choose habitats on the basis of ecological factors and that fitness is expected to decline as density increases (Maynard Smith 1974, Halama and Dueser 1994, Ovadia and Abramsky 1995). Yet the evidence that individuals overwhelmingly select unsaturated habitats is lean (Stamps 1991). For instance, foraging flocks of mixed species are commonplace in both nonbreeding temperate (Morse 1970, Gaddis 1980, Szekely et al. 1989, Dolby and Grubb 1999) and tropical (Winterbottom 1949, Greig-Smith 1978, Eguchi et al. 1993, Hutto 1994) passerine communities. Although those social factors are not sexual, such patterns indicate that the prevailing determinant of what area to occupy can be social, rather than resource-based.

Social attraction influences far more than foraging groups, however (Smith and Peacock 1990, Reed and Dobson 1993, Doligez et al. 2002). Conspecific attraction, the tendency for an individual to settle near individuals of the same species, influences settlement patterns in many breeding passerines, for example, Pied Flycatchers (Ficedula hypoleuca; Alatalo et al. 1982), Least Flycatchers (E. minimus; Tarof and Ratcliffe 2000), House Wrens (Troglodytes aedon; Muller et al. 1997), Bearded Tits (Panurus biarmicus; Hoi and Hoi-Leitner 1997), Black-capped Chickadees (Poecile atricapillus; Ramsay et al. 1999), and tropical passerines (Collias and Collias 1969). Where breeding territories may be clustered because of conspecific attraction (Stamps 1988, Tarof and Ratcliffe 2004), local breeding density may not be a good predictor of habitat quality for any particular species.

Some contend that conspecific attraction results because new arrivals, in considering their own prospects, assess and rely on the reproductive success of conspecifics as a kind of “public information“ (Forbes and Kaiser 1994, Danchin et al. 1998, Doligez et al. 2002), indirectly selecting for aggregations. As such, the information from such social cues is used to make ecologically advantageous habitat choices. Alternatively, aggregations may be directly selected, as when individuals seek benefits of aggregations such as shared vigilance (Kenward 1978, Popp 1988) or mating opportunities (Wagner 1993, 1998; Hoi and Hoi-Leitner 1997).

Social attraction does not always serve to promote settlement in ecologically advantageous habitats. Muller et al. (1997) concluded in their long-term House Wren study that newcomers established all-purpose territories near conspecifics in preference to isolated territories of equivalent quality, which is similar to the findings of Stamps (1988, 1991) in her studies of anole lizards (Anolis sp.). In reviewing the concept of indirect mate choice, Wiley and Poston (1996) cited work on marine fish (Warner 1988) and lekking birds and mammals (Wiley 1991) in concluding that mating can occur at predetermined locations that have an arbitrary and traditional component. They argued that the advantages of avian nesting aggregations for indirect mate choice could be evolutionarily stable, even though there may be some ecological disadvantage to the location.

Although the concepts of aggregations resulting from mate choosiness (Wagner 1993, 1998; Hoi and Hoi-Leitner 1997) or of aggregations used in indirect mate choice (Wiley and Poston 1996) employ sexual selection thinking, the sexual selection acts to cluster individuals but does not act to define species-specific habitat. Habitat specificity remains an ecologically, not sexually, designed trait.

Why consider sexual selection in explaining habitat patterns?—

Given the (1) prevalence of breeding-habitat specificity, (2) cryptic use of nonbreeding habitats during breeding, (3) tremendous ability to use and occupy multiple habitat types, (4) relaxed or varied habitat preferences during nonbreeding periods, (5) flexibility in resource exploitation, (6) selective pressures exerted during nonbreeding situations, (7) social attraction to other birds both in settling breeding territories and during nonbreeding foraging, and (8) clustered patterns of breeding territories, I suggest that the stereotyped breeding habitat preferences of many migrant passerines are not satisfactorily explained by recourse to ecological selection.

Consider the Kirtland’s Warbler (D. kirtlandii), a rare passerine that exhibits several extreme traits in this regard. It has a small breeding range in central Michigan and winters in the Bahamas. According to Mayfield (1960, 1992), its rarity is primarily a consequence of its small and specialized breeding habitat—young jack pine (Pinus banksiana) woodlands 2–6 m high. Breeding territories are clustered, and tracts that seem marginal are sometimes occupied, whereas others that seem ideal are empty of birds. To assert that a species is adaptively restricted (sensu ecological selection) to such a narrow breeding habitat when it spends one-third or more of its year in Bahaman scrub and several other months in varied migration-route habitats stretches credibility.

The work of Willson and Comet (1996) in bo-real passerine communities provides additional possible examples of birds whose breedinghabitat traits are not sufficiently explained by ecological niche. They found that some breeding birds typically associated with conifers foraged primarily in deciduous foliage; in the cases of Ruby-crowned Kinglet (Regulus calendula) and Hermit Thrush (Catharus guttatus), one or two spruce trees in hardwood situations were frequently enough for territory establishment. One might suggest in such cases that one or two trees can meet a species’ ecological need for conifers, especially if the adaptation is not for foraging (e.g. nest sites; Steele 1993). Yet that leaves us to wonder why such species are normally associated with substantial conifer representation when they can breed as well in deciduous habitats. Ecological release, in which the absence of competitors allows niche expansions (Cox and Ricklefs 1977), is another possible explanation; yet the boreal communities that Willson and Comet (1996) studied included numerous deciduous forest passerines.

When early students of evolution were puzzled by certain physical and behavioral traits that could not easily be explained by ecological selection, sexual selection provided an alternative and largely satisfactory framework for consideration. In considering puzzling aspects of avian breeding-habitat specificity, sexual selection may similarly be of assistance. Could elements of breeding habitat be a sexual commodity? More particularly, could preference for specific breeding habitat be a secondary sexual trait that, in proportion to its degree of manifestation by (1) the obtaining of space within it (by males) or (2) the selection of such males (by females), lends reproductive advantage to those individuals more strongly manifesting it? Even though it seems counterintuitive for an individual to select a site by choosing habitat features that do not optimize ecological opportunities, evolution has altered countless physical and behavioral traits in producing a rich variety of sexually selected systems (Andersson 1994). Provided that such sexual selection pays reproductive dividends, those traits can be neutral or even deleterious with respect to survival. So long as the sexual benefits afforded by one habitat have stronger consequences for reproductive fitness than ecological benefits afforded by alternative habitats, there is no prima facie reason why sexual selection should not exploit breeding habitat as a commodity in sexual relations.

The sexual selection literature is rich in empirical and theoretical studies. Several paradigms have had substantial circulation, and below I assess their applicability to the idea of sexually selected habitat. Three well-established models are direct benefits, indirect benefits, and sensory drive (Kokko et al. 2003). Sexual conflict (Trivers 1972, Parker 1979), which shifts the focus from benefits to costs, and species recognition are other paradigms for considering breeding habitat as a secondary sexual trait. For models that might generate sexually selected breeding habitat, Box 1 demonstrates the manner in which those models could work.

Direct benefits models of sexual selection

In the “good resources“ model, females select males that provide the greatest material benefit or the greatest amelioration of some reproductive cost, conferring an immediate contribution to fitness. Selection can favor males that directly provide valuable gifts to female or young (Wiggins and Morris 1986), or provide supportive territories (e.g. Searcy and Yasukawa 1983) or other defendable resources (Slagsvold 1986). Accordingly, the trait sexually selected itself has intrinsic nonarbitrary benefit or is a badge that honestly advertises a benefit. That makes it difficult to discern the degree to which such a trait is favored by (1) male mating success through sexual selection or (2) reproductive success through ecological selection (Andersson 1994). If habitat were sexually selected in this way, such habitat would be ecologically optimal, not merely ecologically acceptable. That would align habitat parameters favored by ecological and sexual selection, rendering ecological and sexual selection on habitat features concordant and, hence, indistinguishable.

Indirect benefits models

Indirect sexual selection occurs where there is direct selection on a trait that is genetically correlated with the secondary sexual trait (Kokko et al. 2003). There are two principal mechanisms. The “Fisherian“ or “runaway“ model (Fisher 1930, O’Donald 1980) produces sexual traits that are nonadaptive, except with respect to mating. An initial advantage not due to sexual preference (sensu ecological selection) and a subsequent second advantage conferred by female preference conspire to concentrate in offspring both the preference and the trait. The intensity of such self-reinforcing selection increases so long as the sons of females exercising the preference have an advantage over other males, and the trait develops to the point where some non-sexual disadvantage counterbalances the sexual advantage (Schluter et al. 1991).

i0004-8038-122-2-689-ex1.gif

A male tendency to obtain a territory in an advantaged habitat (sensu ecological selection) coupled to a female tendency to prefer such males could satisfy Fisher’s two selective influences, generating sexually selected habitat. Both (1) the initial advantage conferred by the habitat trait and (2) the trait itself might be modest, but the latter could be multiplied many-fold by run-away selection stemming from the correlated preference trait. Countering ecological selection would prevent the narrowing of selected habitat parameters to points where the sexually selected habitat becomes excessively costly by being too rare, too unproductive, too narrowly circumscribed, or too excessively represented by the selected trait. Theoreticians do not agree on whether traits sculpted by Fisherian sexual selection are sustainable when female reproductive success is compromised (see Lande 1981, Kirkpatrick 1985, Pomiankowski et al. 1991, Day 2000). If not sustainable, this model could generate sexually selected habitat boundaries, but not ones that are costly to females.

The second indirect hypothesis is the “good genes“ model: the sexually selected trait is costly but is coupled with some trait-enhancing survival. Females select costly male traits because they honestly signify high heritable viability (e.g. Zahavi 1975, Møller 1991, Petrie 1992; but see Brooks 2000), instead of being arbitrarily attractive as in Fisherian sexual selection. Although such indicators may also have nonsexual benefits (e.g. large size), ecologically selected and sexually selected optima are unlikely to be or remain the same, entailing a cost to sexual selection. Kirkpatrick (1996) showed theoretically that the good genes model can in some circumstances be costly for females, especially if countering ecological selection is weak.

For a sexually selected habitat trait to be an indicator of good genes, a correlation is required between heritable beneficial traits and a male’s ability to settle in sexually prescribed habitat. That could be satisfied by male vigor; males most able to commandeer coveted sites would be those that can, in comparison with others, migrate earliest, defend best, display most effectively, and survive. By virtue of the specific habitat being a sexual commodity subject to competition, females’ ultimate preference for good genes is mediated by a proximate preference for males occupying specific habitat. That system would select for and entrench that specificity, with ecological selection tending to counter the development of excessively narrow habitat requirements.

Sensory drive and species recognition

Ecological selection for sensory sensitivity to particular colors or shapes may produce a mating bias favoring sexual traits reminiscent of such colors or shapes (referred to as, among other names, the “sensory drive“ model; e.g. Endler and Basolo 1998, Rodd et al. 2001). Sensory drive may be the “nudge“ required to get a sexually selected system going (Kokko et al. 2003). Habitat parameters are much more complex than the colors or shapes exploited by sensory drive, however, making the sexually selected entrenchment of a particular breeding habitat through sensory drive unlikely. Although it is true that sexually selected traits like song frequency or plumage color can be dependent on environmental context (Hunter and Krebs 1979, Boughman 2002), that is not the same as suggesting that those traits determine environmental context by prescribing specific habitat.

In the “species recognition“ model, it is contended that secondary sexual traits may be selected because they promote conspecific mate choice (Wallace 1889, Sibley 1957, Maynard Smith 1978). Regardless of the evidence, it is implausible that such a process could favor sexually selected habitat, because there are much better ways of recognizing a conspecific than assessing the habitat it occupies. Sexually selected habitat generated by other mechanisms may play a role in speciation or reproductive isolation, however. Ten Cate and Bateson (1988) suggested that assortative mating favored by diverging secondary sexual traits between populations could drive speciation. If one accepts the argument of Rice (1987) that sympatric speciation could flow from disruptive ecological selection on a habitat trait, there is no reason why disruptive sexual selection on a habitat trait could not similarly drive sympatric speciation.

Sexual conflict

Evidence for sexual conflict, the divergence between male and female reproductive interests, has been accumulating (Parker 1979, Arnqvist and Rowe 2002, Chapman et al. 2003). Modeling indicates that such antagonism can prevent each sex from reaching sex-specific optima, reducing overall population fitness (Gavrilets et al. 2001). Sexual conflict can impair female fitness if the optimal expression of a trait differs between the sexes (Rice and Chippindale 2001) or if a male trait increases the male’s paternity, notwithstanding that such increase may decrease a female’s reproductive output (Civetta and Clark 2000, Crudgington and Siva-Jothy 2000).

Sexual conflict can be facilitated by dimorphism under a “divergence in trait-optima“ model. To the extent that morphology determines optimal habitat, such dimorphism could generate a sexual divergence in what constitutes optimal habitat. Different preferred winter habitats based on sex have been reported for passerines (Power 1980, Lynch et al. 1985). If habitat optima differ between the sexes, breeding habitat may reflect more the optimum of the controlling sex (presumably the choosing females) than that of the noncontrolling sex, entailing a cost to the latter. Accordingly, if during breeding the noncontrolling sex occupies the optimal habitat of the controlling sex, sexual dynamics are modestly influencing habitat choice. Ecological selection on the controlling sex and sexual selection (through conflict) on the noncontrolling sex prescribe specific breeding habitat.

The second conflict model that might affect habitat specificity is a “territorial aggregation“ model, in which specific habitat is chosen not for resource exploitation but for the promotion of aggregation. Males commonly show substantially more variance than females in reproductive success (Clutton-Brock and Vincent 1991) through male-biased sex ratios (Stewart and Aldrich 1951, Smith 1978), polygyny, and especially extrapair copulations (Westneat et al. 1990, Møller and Cuervo 2000). Such nonmonogamous mating systems tend to affect female fitness qualitatively through female choice. In hidden leks (Wagner 1998), pursuit of extrapair males by females (Neudorf et al. 1997) selects for aggregations of male territories by rewarding males that tend to establish territories near other males (Hoi and Hoi-Leitner 1997).

Ecological selection is expected to concentrate male territories in habitat suitable for resource exploitation, but mate-choice rewards for females owing to such aggregation could narrow the habitat specificity. Because females seek access to multiple males to exercise choice, sexual selection will favor male traits that lead to aggregations, and the narrowing of habitat parameters over which males compete could lead to such increased aggregation. Consequently, fitness benefits to females through access to superior males could entrench a sexually selected habitat (sensu sexual conflict) by virtue of the correlation between habitat specificity and such mating opportunities. Alternatively, if aggregation of male territories is driven not by females but by superior males, habitat specificity could be entrenched in a similar way.

Conclusions

Although researchers continue to look to ecological selection as the primary explanation of habitat specificity, there is no prima facie reason why sexual selection might not influence breeding habitat preferences. Good resources, sensory drive, and species recognition models of sexual selection are unlikely to be primary forces in influencing habitat specificity in organisms. The “divergence in traitoptima“ sexual-conflict model might modestly influence habitat specificity for one sex, though ecological habitat selection prevails through the other sex.

However, indirect sexual-selection models (Fisherian and good genes) and a “territorial aggregation“ sexual-conflict model may be primary forces. In particular, such forces may work to generate habitat preferences that are not primarily mediated by the niche concerns of ecological selection. The significance of defending specific habitats when habitat is sexually selected is not that such territories provide resources in a manner superior to territories in alternative habitats, but that the habitat itself constitutes the currency of male competition and female choice.

Acknowledgments

I thank J. Rising and D. Jackson for advice throughout my doctoral work, of which this forms a part. E. Dunn, H. Rodd, and two anonymous reviewers made substantial contributions to restructuring and reconceiving the first draft. I also thank T. Rising and C. Mills for manuscript assistance, and L. Rowe for discussions regarding sexual selection and sexual conflict. I was supported by a Natural Sciences and Engineering Research Council (NSERC) postgraduate scholarship (Canada), the Department of Zoology at the University of Toronto, and by Donald Jackson’s operating NSERC grant.

Literature Cited

1.

R. V. Alatalo, A. Lundberg, and M. Bjorklund . 1982. Can the song of male birds attract other males? An experiment with the Pied Flycatcher Ficedula hypoleuca. Bird Behaviour 4:42–45. Google Scholar

2.

A. D. Anders, J. Faaborg, and F. R. Thompson III . 1998. Postfledging dispersal, habitat use, and home-range size of juvenile Wood Thrushes. Auk 115:349–358. Google Scholar

3.

M. Andersson 1994. Sexual Selection. Princeton University Press, Princeton, New Jersey.  Google Scholar

4.

G. Arnqvist and L. Rowe . 2002. Antagonistic coevolution between the sexes in a group of insects. Nature 415:787–789. Google Scholar

5.

F. Bairlein 1980. Ecosystem analysis of resting areas of migratory birds: Description and interpretation of trapping stations of the “Mettnau-Reit-Illmitz-Program.“. Okologie der Vogel 3:7–137. Google Scholar

6.

A-M. Benson and K. Winker . 2001. Timing of breeding range occupancy among highlatitude passerine migrants. Auk 118:513–519. Google Scholar

7.

J. W. Boughman 2002. How sensory drive can promote speciation. Trends in Ecology and Evolution 17:571–577. Google Scholar

8.

R. Brooks 2000. Negative genetic correlation between male sexual attractiveness and survival. Nature 406:67–70. Google Scholar

9.

J. H. Brown, D. W. Mehlman, and G. C. Stevens . 1995. Spatial variation in abundance. Ecology 76:2028–2043. Google Scholar

10.

R. E. Brown and J. G. Dickson . 1994. Swainson’s Warbler (Limnothlypis swainsonii). In The Birds of North America, no. 126 (A. Poole and F. Gill, Eds.). Academy of Natural Sciences, Philadelphia, and American Ornithologists’ Union, Washington, D.C.  Google Scholar

11.

D. G. Busby and S. G. Sealy . 1979. Feeding ecology of a population of nesting Yellow Warblers. Canadian Journal of Zoology 57:1670–1681. Google Scholar

12.

T. Chapman, G. Arnqvist, J. Bangham, and L. Rowe . 2003. Sexual conflict. Trends in Ecology and Evolution 18:41–47. Google Scholar

13.

N. Chernetsov 2002. Foraging strategies of migrating Reed and Sedge warblers. Page 313 in Acta XXIII Congressus Internationalis Ornithologici. Beijing, China.  Google Scholar

14.

A. Civetta and A. G. Clark . 2000. Correlated effects of sperm competition and postmating female mortality. Proceedings of the National Academy of Sciences USA 97:13162–13165. Google Scholar

15.

T. H. Clutton-Brock and A. C J. Vincent . 1991. Sexual selection and the potential reproductive rates of males and females. Nature 351:58–60. Google Scholar

16.

N. E. Collias and E. C. Collias . 1969. Size of breeding colony related to attraction of mates in a tropical passerine bird. Ecology 50:481–488. Google Scholar

17.

J. L. Confer and J. L. Larkin . 1999. Behavioral interactions between Golden-winged and Blue-winged warblers. Auk 115:209–214. Google Scholar

18.

G. W. Cox and R. E. Ricklefs . 1977. Species diversity and ecological release in Caribbean land bird faunas. Oikos 28:113–122. Google Scholar

19.

H. S. Crudgington and M. T. Siva-Jothy . 2000. Genital damage, kicking and early death: The battle of the sexes takes a sinister turn in the bean weevil. Nature 407:855–856. Google Scholar

20.

E. Danchin, T. Boulinier, and M. Massot . 1998. Conspecific reproductive success and breeding habitat selection: Implications for the study of coloniality. Ecology 79:2415–2428. Google Scholar

21.

T. Day 2000. Sexual selection and the evolution of costly female preferences: Spatial effects. Evolution 54:715–730. Google Scholar

22.

D. M. Debinski and P. F. Brussard . 1994. Using biodiversity data to assess species-habitat relationships in Glacier National Park, Montana. Ecological Applications 4:833–843. Google Scholar

23.

A. S. Dolby and T. C. Grubb Jr. . 1999. Functional roles in mixed-species foraging flocks: A field manipulation. Auk 116:557–559. Google Scholar

24.

B. Doligez, E. Danchin, and J. Clobert . 2002. Public information and breeding habitat selection in a wild bird population. Science 297:1168–1170. Google Scholar

25.

J. L. Dunn and K. L. Garrett . 1997. A Field Guide to Warblers of North America. Houghton Mifflin, Boston.  Google Scholar

26.

K. Eguchi, S. Yamagishi, and V. Randianasolo . 1993. The composition and foraging behaviour of mixed-species flocks of forest-living birds in Madagascar. Ibis 135:91–96. Google Scholar

27.

J. A. Endler and A. L. Basolo . 1998. Sensory ecology, receiver biases and sexual selection. Trends in Ecology and Evolution 13:415–420. Google Scholar

28.

B. J. Ens, M. Kersten, A. Brenninkmeijer, and J. B. Hulscher . 1992. Territory quality, parental effort and reproductive success of Oystercatchers (Haematopus ostralegus). Journal of Animal Ecology 61:703–715. Google Scholar

29.

K. L. Evans, R. B. Bradbury, and J. Wilson . 2002. Population trends and the role of habitat quality in limiting populations of Barn Swallows in Britain. Page 128 in Acta XXIII Congressus Internationalis Ornithologici. Beijing, China.  Google Scholar

30.

R. A. Fisher 1930. The Genetical Theory of Natural Selection. Clarendon Press, Oxford, United Kingdom.  Google Scholar

31.

J. A D. Flack 1976. Bird populations of aspen forests in western North America. Ornithological Monographs, no. 19.  Google Scholar

32.

L. S. Forbes and G. W. Kaiser . 1994. Habitat choice in breeding seabirds: When to cross the information barrier. Oikos 70:377–384. Google Scholar

33.

S. D. Fretwell and H. L. Lucas . 1970. On territorial behavior and other factors influencing habitat distribution in birds. I. Theoretical development. Acta Biotheoretica 19:16–36. Google Scholar

34.

P. Gaddis 1980. Mixed flocks, accipiters, and antipredator behavior. Condor 82:348–349. Google Scholar

35.

S. Gavrilets, G. Arnqvist, and U. Friberg . 2001. The evolution of female mate choice by sexual conflict. Proceedings of the Royal Society of London, Series B 268:531–539. Google Scholar

36.

N. J. Gotelli, N. J. Buckley, and J. A. Wiens . 1997. Co-occurrence of Australian land birds: Diamond’s assembly rules revisited. Oikos 80:311–324. Google Scholar

37.

P. W. Greig-Smith 1978. The formation, structure and function of mixed-species insectivorous flocks in west African savanna woodland. Ibis 120:284–295. Google Scholar

38.

K. J. Halama and R. D. Dueser . 1994. Of mice and habitats: Tests for density-dependent habitat selection. Oikos 69:107–114. Google Scholar

39.

H. Hoi and M. Hoi-Leitner . 1997. An alternative route to coloniality in the Bearded Tit: Females pursue extra-pair fertilizations. Behavioral Ecology 8:113–119. Google Scholar

40.

R. T. Holmes 1986. Foraging patterns of forest birds: Male-female differences. Wilson Bulletin 98:196–213. Google Scholar

41.

R. T. Holmes 1994. Black-throated Blue Warbler (Dendroica caerulescens). In The Birds of North America, no. 87 (A. Poole and F. Gill, Eds.). Academy of Natural Sciences, Philadelphia, and American Ornithologists’ Union, Washington, D.C.  Google Scholar

42.

R. T. Holmes, P. P. Marra, and T. W. Sherry . 1996. Habitat-specific demography of breeding Black-throated Blue Warblers (Dendroica caerulescens): Implications for population dynamics. Journal of Animal Ecology 65:183–195. Google Scholar

43.

M. L. Hunter Jr. and J. R. Krebs . 1979. Geographical variation in the song of the Great Tit (Parus major) in relation to ecological factors. Journal of Animal Ecology 48:759–785. Google Scholar

44.

R. L. Hutto 1994. The composition and social organization of mixed-species flocks in a tropical deciduous forest in western Mexico. Condor 96:105–118. Google Scholar

45.

F. C. James 1982. The ecological morphology of birds: A review. Annales Zoologici Fennici 19:265–275. Google Scholar

46.

J. Jones and R. J. Robertson . 2001. Territory and nest-site selection of Cerulean Warblers in eastern Ontario. Auk 118:727–735. Google Scholar

47.

M. Katti and T. Price . 1999. Annual variation in fat storage by a migrant warbler over-wintering in the Indian tropics. Journal of Animal Ecology 68:815–823. Google Scholar

48.

T. E. Katzner, E. A. Bragin, S. T. Knick, and A. T. Smith . 2003. Coexistence in a multispecies assemblage of eagles in central Asia. Condor 105:538–551. Google Scholar

49.

R. E. Kenward 1978. Hawks and doves: Factors affecting success and selection in goshawk attacks on wood pigeons. Journal of Animal Ecology 47:449–460. Google Scholar

50.

D. I. King, C. R. Griffin, P. J. Champlin, and T. B. Champlin . 2000. An evaluation of the use of the Nature Conservancy Vegetation Classification for mapping bird distribution at Chincoteague National Wildlife Refuge. Natural Areas Journal 20:78–84. Google Scholar

51.

D. A. Kirk and K. A. Hobson . 2001. Bird-habitat relationships in jack pine boreal forests. Forest Ecology and Management 147:217–243. Google Scholar

52.

M. Kirkpatrick 1985. Evolution of female choice and male parental investment in polygynous speices: The demise of the “sexy son“. American Naturalist 125:788–810. Google Scholar

53.

M. Kirkpatrick 1996. Good genes and direct selection in the evolution of mating preferences. Evolution 50:2125–2140. Google Scholar

54.

H. Kokko, R. Brooks, M. Jennions, and J. Morley . 2003. The evolution of mate choice and mating biases. Proceedings of the Royal Society of London, Series B 270:653–664. Google Scholar

55.

J. R. Krebs 1971. Territory and breeding density in the Great Tit Parus major L. Ecology 52:2–22. Google Scholar

56.

D. Lack 1943. The Life of the Robin. H. F. and G. Witherby, London.  Google Scholar

57.

A. B. Lambert 1987. Prairie Warbler. In Atlas of the Breeding Birds of Ontario (M. D. Cadman, P. F. J. Eagles, and F. M. Helleiner, Eds.). University of Waterloo Press, Waterloo, Ontario.  Google Scholar

58.

R. Lande 1981. Models of speciation by sexual selection on polygenic traits. Proceedings of the National Academy of Sciences USA 78:3721–3725. Google Scholar

59.

S. C. Latta and J. Faaborg . 2002. Demographic and population responses of Cape May Warblers wintering in multiple habitats. Ecology 83:2502–2515. Google Scholar

60.

B. Leisler 1980. Morphological aspects of ecological specialization in bird genera. Okologie der Vogel 2:199–200. Google Scholar

61.

I. J. Lovette and R. T. Holmes . 1995. Foraging behavior of American Redstarts in breeding and wintering habitats: Implications for relative food availability. Condor 97:728–791. Google Scholar

62.

G. A. Lozano and R. E. Lemon . 1998. Parental-care responses by Yellow Warblers (Dendroica petechia) to simultaneous manipulations of food abundance and brood size. Canadian Journal of Zoology 76:916–924. Google Scholar

63.

J. F. Lynch, E. S. Morton, and M. E. Van der Voort . 1985. Habitat segregation between the sexes of wintering Hooded Warblers (Wilsonia citrina). Auk 102:714–721. Google Scholar

64.

R. H. MacArthur 1958. Population ecology of some warblers of northeastern coniferous forests. Ecology 39:599–619. Google Scholar

65.

R. H. MacArthur, J. W. MacArthur, and J. Preer . 1962. On bird species diversity. II. Prediction of bird census from habitat measurement. American Naturalist 96:167–174. Google Scholar

66.

R. MacNally 2000. Coexistence of a locally undifferentiated foraging guild: Avian snatchers in a southeastern Australian forest. Austral Ecology 25:69–82. Google Scholar

67.

B. A. Maurer and R. C. Whitmore . 1981. Foraging of five bird species in two forests with different vegetation structure. Wilson Bulletin 93:478–490. Google Scholar

68.

D. J. May 1949. Studies on a community of Willow Warblers. Ibis 91:24–54. Google Scholar

69.

H. Mayfield 1960. The Kirtland’s Warbler. Cranbrook Institute of Science, Bloomfield Hills, Michigan.  Google Scholar

70.

H. F. Mayfield 1992. Kirtland’s Warbler (Dendroica kirtlandii). In The Birds of North America, no. 19 (A. Poole, P. Stettenheim, and F. Gill, Eds.). Academy of Natural Sciences, Philadelphia, and American Ornithologists’ Union, Washington, D.C.  Google Scholar

71.

J. Maynard Smith 1974. Models in Ecology. Cambridge University Press, Cambridge, United Kingdom.  Google Scholar

72.

J. Maynard Smith 1978. The Evolution of Sex. Cambridge University Press, Cambridge, United Kingdom.  Google Scholar

73.

B. J. McCaffery 1998. Implications of frequent habitat switches in foraging Bar-tailed Godwits. Auk 115:494–497. Google Scholar

74.

S. K. McKnight and G. R. Hepp . 1998. Foragingniche dynamics of Gadwalls and American Coots in winter. Auk 115:670–683. Google Scholar

75.

B. McMartin, I. Bellocq, and S. M. Smith . 2002. Patterns of consumption and diet differentiation for three breeding warbler species during a spruce budworm outbreak. Auk 119:216–220. Google Scholar

76.

A. P. Møller 1991. Viability is positively related to degree of ornamentation in male swallows. Proceedings of the Royal Society of London, Series B 243:145–148. Google Scholar

77.

A. P. Møller and J. J. Cuervo . 2000. The evolution of paternity and paternal care in birds. Behavioral Ecology 11:472–485. Google Scholar

78.

D. H. Morse 1970. Ecological aspects of some mixed-species foraging flocks of birds. Ecological Monographs 40:119–168. Google Scholar

79.

D. H. Morse 1989. American Warblers. An Ecological and Behavioral Perspective. Harvard University Press, Cambridge, Massachusetts.  Google Scholar

80.

K. L. Muller, J. A. Stamps, V. V. Krishnan, and N. H. Willits . 1997. The effects of conspecific attraction and habitat quality on habitat selection in territorial birds (Troglodytes aedon). American Naturalist 150:650–661. Google Scholar

81.

M. T. Murphy, A. Pierce, J. Shoen, K. L. Murphy, J. A. Campbell, and D. A. Hamilton . 2001. Population structure and habitat use by overwintering Neotropical migrants on a remote oceanic island. Biological Conservation 102:333–345. Google Scholar

82.

D. L. Neudorf, B. J M. Stutchbury, and W. H. Piper . 1997. Covert extraterritorial behavior of female Hooded Warblers. Behavioral Ecology 8:595–600. Google Scholar

83.

I. Newton 2004. Population limitation in migrants. Ibis 146:197–226. Google Scholar

84.

M. Nice 1937. Studies on the life history of the Song Sparrow. Transactions of the Linnaean Society of New York, no. 4.  Google Scholar

85.

V. Nolan Jr. 1978. The ecology and behavior of the Prairie Warbler Dendroica discolor. Ornithological Monographs, no. 26.  Google Scholar

86.

D. R. Norris, P. P. Marra, T. K. Kyser, T. W. Sherry, and L. M. Ratcliffe . 2004. Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird. Proceedings of the Royal Society of London, Series B 271:59–64. Google Scholar

87.

P. O’Donald 1980. Genetic models of sexual and natural selection in monogamous organisms. Heredity 44:391–415. Google Scholar

88.

O. Ovadia and Z. Abramsky . 1995. Density-dependent habitat selection: Evaluation of the isodar method. Oikos 73:86–94. Google Scholar

89.

R. W. Pagen, F. R. Thompson III, and D. E. Burhans . 2000. Breeding and post-breeding habitat use by forest migrant songbirds in the Missouri Ozarks. Condor 102:738–747. Google Scholar

90.

G. A. Parker 1979. Sexual selection and sexual conflict. Pages 123–166 in Sexual Selection and Reproductive Competition in Insects (M. S. Blum and N. A. Blum, Eds.). Academic Press, New York.  Google Scholar

91.

C. A. Paszkowski 1984. Macrohabitat use, microhabitat use, and foraging behavior of the Hermit Thrush and Veery in a northern Wisconsin forest. Wilson Bulletin 96:286–292. Google Scholar

92.

M. Petrie 1992. Peacocks with low mating success are more likely to suffer predation. Animal Behaviour 44:585–586. Google Scholar

93.

V. Polo and L. M. Carrascal . 1999. Shaping the body mass distribution of passeri-formes: Habitat use and body mass are evolutionarily and ecologically related. Journal of Animal Ecology 68:324–337. Google Scholar

94.

A. Pomiankowski, Y. Iwasa, and S. Nee . 1991. The evolution of costly mate preferences. I. Fisher and biased mutation. Evolution 45:1422–1430. Google Scholar

95.

J. W. Popp 1988. Scanning behavior of finches in mixed-species groups. Condor 90:510–512. Google Scholar

96.

H. W. Power 1980. The foraging behavior of Mountain Bluebirds with emphasis on sexual foraging differences. Ornithological Monographs, no. 28.  Google Scholar

97.

S. M. Ramsay, K. Otter, and L. M. Ratcliffe . 1999. Nest-site selection by female Black-capped Chickadees: Settlement based on conspecific attraction? Auk 116:604–617. Google Scholar

98.

J. M. Reed and A. P. Dobson . 1993. Behavioral constraints and conservation biology: Conspecific attraction and recruitment. Trends in Ecology and Evolution 8:253–256. Google Scholar

99.

W. R. Rice 1987. Speciation via habitat specialization: The evolution of reproductive isolation as a correlated character. Evolutionary Ecology 1:301–314. Google Scholar

100.

W. R. Rice and A. K. Chippindale . 2001. Intersexual ontogenetic conflict. Journal of Evolutionary Biology 14:685–693. Google Scholar

101.

F. H. Rodd, K. A. Hughes, G. F. Grether, and C. T. Baril . 2001. A possible non-sexual origin of a mate preference: Are male guppies mimicking fruit? Proceedings of the Royal Society of London, Series B 269:475–481. Google Scholar

102.

M. L. Rosenzweig 1991. Habitat selection and population interactions: The search for mechanism. American Naturalist 137 (Supplement):. 5–28. Google Scholar

103.

J. T. Rotenberry and J. A. Wiens . 1998. Foraging patch selection by shrubsteppe sparrows. Ecology 79:1160–1173. Google Scholar

104.

J. M. Ruth and T. R. Stanley . 2002. Breeding habitat use by sympatric and allopatric populations of Wilson’s Warblers and Yellow Warblers. Journal of Field Ornithology 73:412–419. Google Scholar

105.

D. Schluter, T. D. Price, and L. Rowe . 1991. Conflicting selection pressures and life history trade-offs. Proceedings of the Royal Society of London, Series B 246:11–17. Google Scholar

106.

W. A. Searcy and K. Yasukawa . 1983. Sexual selection and Red-winged Blackbirds. American Scientist 71:166–174. Google Scholar

107.

R. K. Selander 1966. Sexual dimorphism and differential niche utilization in birds. Condor 68:113–151. Google Scholar

108.

E. Shochat, Z. Abramsky, B. Pinshow, and M. E A. Whitehouse . 2002. Density-dependent habitat selection in migratory passerines during stopover: What causes the deviation from IFD? Evolutionary Ecology 16:469–488. Google Scholar

109.

C. G. Sibley 1957. The evolutionary and taxonomic significance of sexual dimorphism and hybridization in birds. Condor 59:166–191. Google Scholar

110.

T. Slagsvold 1986. Nest settlement by the Pied Flycatcher: Does the female choose her mate for the quality of his house or himself? Ornis Scandinavica 17:210–220. Google Scholar

111.

A. T. Smith and M. M. Peacock . 1990. Conspecific attraction and the determination of metapopulation colonization rates. Conservation Biology 4:320–323. Google Scholar

112.

S. M. Smith 1978. The “underworld“ in a territorial sparrow: Adaptive strategy for floaters. American Naturalist 112:571–582. Google Scholar

113.

J. A. Stamps 1988. Conspecific attraction and aggregation in territorial birds. American Naturalist 131:329–347. Google Scholar

114.

J. A. Stamps 1991. The effect of conspecifics on habitat selection in territorial species. Behavioral Ecology and Sociobiology 28:29–36. Google Scholar

115.

B. B. Steele 1993. Selection of foraging and nesting sites by Black-throated Blue Warblers: Their relative influence on habitat choice. Condor 95:568–579. Google Scholar

116.

R. E. Stewart and J. W. Aldrich . 1951. Removal and repopulation of breeding birds in a spruce-fir forest community. Auk 68:471–482. Google Scholar

117.

A. M. Strong and T. W. Sherry . 2000. Habitat-specific effects of food abundance on the condition of Ovenbirds wintering in Jamaica. Journal of Animal Ecology 69:883–895. Google Scholar

118.

T. Szekely, T. Szep, and T. Juhasz . 1989. Mixed species flocking of tits (Parus spp.): A field experiment. Oecologia 78:490–495. Google Scholar

119.

S. A. Tarof and L. M. Ratcliffe . 2000. Pair formation and copulation behavior in Least Flycatcher clusters. Condor 102:832–837. Google Scholar

120.

S. A. Tarof and L. M. Ratcliffe . 2004. Habitat characteristics and nest predation do not explain clustered breeding in Least Flycatchers (Empidonax minimus). Auk 121:877–893. Google Scholar

121.

C. Ten Cate and P. Bateson . 1988. Sexual selection: The evolution of conspicuous characteristics in birds by means of imprinting. Evolution 42:1355–1358. Google Scholar

122.

J-M. Thiollay 1988. Comparative foraging success of insectivorous birds in tropical and temperate forests: Ecological implications. Oikos 53:17–30. Google Scholar

123.

I. Tremblay, D. W. Thomas, M. M. Lambrechts, J. Blondel, and P. Perret . 2003. Variation in Blue Tit breeding performance across gradients in habitat richness. Ecology 84:3033–3043. Google Scholar

124.

R. L. Trivers 1972. Parental investment and sexual selection. Pages 136–179 in Sexual Selection and the Descent of Man 1871–1971 (B. Campbell, Ed.). Aldine Publishing Company, Chicago, Illinois.  Google Scholar

125.

R. H. Wagner 1993. The pursuit of extra-pair copulations by female birds: A new hypothesis of colony formation. Journal of Theoretical Biology 163:333–346. Google Scholar

126.

R. H. Wagner 1998. Hidden leks: Sexual selection and the clustering of avian territories. Pages 123–145 in Avian Reproductive Tactics: Female and Male Perspectives (P. G. Parker and N. T. Burley, Eds.). Ornithological Monographs, no. 49.  Google Scholar

127.

A. R. Wallace 1889. Darwinism, 2nd ed. Macmillan, London.  Google Scholar

128.

Y. Wang and D. M. Finch . 2002. Consistency of mist netting and point counts in assessing landbird species richness and relative abundance during migration. Condor 104:59–72. Google Scholar

129.

R. R. Warner 1988. Traditionality of mating-site preferences in a coral reef fish. Nature 335:719–721. Google Scholar

130.

D. A. Welsh and S. C. Lougheed . 1996. Relationships of bird community structure and species distributions to two environmental gradients in the northern boreal forest. Ecography 19:194–208. Google Scholar

131.

D. F. Westneat, P. W. Sherman, and M. L. Morton . 1990. The ecology and evolution of extra-pair copulations in birds. Pages 331– 369 in Current Ornithology, vol. 7 (D. M. Powers, Ed.). Plenum Press, New York.  Google Scholar

132.

J. A. Wiens 1977. On competition and variable environments. American Scientist 65:590–597. Google Scholar

133.

D. A. Wiggins and R. D. Morris . 1986. Criteria for female choice of mates: Courtship feeding and paternal care in the Common Tern. American Naturalist 128:126–129. Google Scholar

134.

R. H. Wiley 1991. Lekking in birds and mammals: Behavioral and evolutionary issues. Advances in the Study of Behavior 20:201–291. Google Scholar

135.

R. H. Wiley and J. Poston . 1996. Perspective: Indirect mate choice, competition for mates, and coevolution of the sexes. Evolution 50:1371–1381. Google Scholar

136.

M. F. Willson and T. A. Comet . 1996. Bird communities of northern forests: Patterns of diversity and abundance. Condor 98:337–349. Google Scholar

137.

J. M. Winterbottom 1949. Mixed bird parties in the tropics, with special reference to northern Rhodesia. Auk 66:258–263. Google Scholar

138.

J. M. Wunderle Jr. and R. B. Waite . 1993. Distribution of overwintering Nearctic migrants in the Bahamas and Greater Antilles. Condor 95:904–933. Google Scholar

139.

R. Yosef and T. C. Grubb Jr. . 1994. Resource dependence and territory size in Loggerhead Shrikes (Lanius ludovicianus). Auk 111:465–469. Google Scholar

140.

A. Zahavi 1975. Mate selection: A selection for a handicap. Journal of Theoretical Biology 53:205–214. Google Scholar

Appendices

Alexander M. Mills "CAN BREEDING HABITAT BE SEXUALLY SELECTED?," The Auk 122(2), 689-700, (1 April 2005). https://doi.org/10.1642/0004-8038(2005)122[0689:CBHBSS]2.0.CO;2
Received: 21 May 2003; Accepted: 20 October 2004; Published: 1 April 2005
JOURNAL ARTICLE
12 PAGES


SHARE
ARTICLE IMPACT
Back to Top