Reproductive Anatomy and Indices of Quality in Male Tree Swallows: the Potential Reproductive Role of Floaters

—Avian populations often consist of breeding residents and nonbreeding floaters. It is usually assumed that floaters are lower-quality individuals that do not reproduce, but floater tactics and potential reproductive success have rarely been examined carefully. To assess the potential reproductive role of male floaters in Tree Swallows (Tachycineta bicolor), we compared their reproductive organs and morphology with those of resident males. Tree Swallows show high levels of extrapair paternity, but two studies attempting to find the fathers of the extrapair offspring have been remarkably unsuccessful. Floater males that father extrapair young would face intense sperm competition. Theory predicts that under intense sperm competition, selection favors males that produce more sperm. Comparative studies in birds and other taxa provide evidence that the level of sperm competition influences relative testes size and sperm production. However, intraspecific adaptations to different levels of sperm competition have received far less attention. Floater Tree Swallows did not differ from resident males in any of the characters we measured, including testes size, but floaters had significantly larger cloacal protuberances. Thus, our results do not confirm the general assumption that floaters are lower-quality individuals that do not reproduce. Furthermore, floaters showed high variation in the volume of the cloacal protuberance (reflecting sperm numbers), which suggests that they engage in copulations. We conclude that floater male Tree Swallows invest heavily in sperm production (as do resident males) to exploit breeding opportunities through takeovers or extrapair copulations. Received 17 November 1998, accepted 5 May 1999. IN SPECIES with internal fertilization, sperm competition occurs when the sperm of two or more males are present in the female reproductive tract and compete for fertilization of the eggs (Parker 1970). Most bird species are socially monogamous, but extrapair copulations (EPCs) leading to extrapair paternity are widespread (Westneat and Webster 1994, Gowaty 1996, Petrie and Kempenaers 1998). Thus, a pair male’s sperm often has to compete with sperm of other males. Theoretical and empirical studies have predicted or shown that factors such as sperm numbers, sperm quality, and the timing of insemination relative to oviposition influence a male’s fertilization success (e.g. Parker 1984, Birkhead et al. 1995b, Colegrave et al. 1995, Birkhead and Biggins 1998). All experimental studies to date have been done on 3 Address correspondence to this author at: Research Center for Ornithology, Max-Planck Society, Postfach 1564, D-82305 Seewiesen, Germany. E-mail: [email protected] domestic birds, and the relative importance of these factors in wild birds is still unknown. Comparative studies show that species with high levels of sperm competition have relatively larger testes, bigger cloacal protuberances, and longer sperm (Briskie and Montgomerie 1992, Birkhead et al. 1993, Møller and Briskie 1995, Briskie et al. 1997). The first two can be seen as adaptations to produce larger ejaculates, as would be expected if sperm competition is a strong selective force. Most studies have focused on interspecific differences in male adaptations to sperm competition. However, individuals of one species may face different levels of sperm competition, leading to differential investment in sperm production (Stockley and Purvis 1993, Stockley et al. 1994, Gage et al. 1995). In birds, such different reproductive tactics are not documented, but a population often consists of breeding residents and a substantial number of nonbreeding floaters. In contrast to breeding individuals, the behavioral tactics and potential reproJanuary 2000] 75 Reproductive Role of Floaters ductive success of floaters have received little attention. Past studies have shown or suggested that floaters are younger, lower-quality, or subordinate individuals that are excluded from breeding by dominant residents (Smith and Arcese 1989, Mönkkönen 1990, Lozano 1994). Thus, it is often assumed that floaters do not reproduce at all. Alternatively, floaters may reproduce by engaging in extrapair copulations. Floaters often are difficult to observe, but one way to elucidate their reproductive role is to study their reproductive anatomy. If floaters are indeed subordinate or lower-quality individuals, we expect their testes to be relatively small or undeveloped. They would have little or no chance to fertilize eggs because females are unlikely to perform extrapair copulations with such males (Smith 1988, Houtman 1992, Kempenaers et al. 1992, Møller 1992). By not investing in gamete production, floaters can save energy for the next breeding season. On the other hand, if floaters pursue an alternative tactic (i.e. reproduce exclusively by performing EPCs), their reproductive organs should be bigger than those of the residents. Floaters would be exposed to higher levels of sperm competition because their sperm always have to compete with those of resident males, whereas not all residents are paired to females that engage in EPCs (Møller and Briskie 1995). Furthermore, within-pair copulations are probably more frequent than EPCs, and pair males would thus have an advantage in terms of number of sperm transferred. Because floaters do not have to engage in energetically costly territorial defense, they could invest more in sperm production to make up for this difference by means of larger ejaculates. Tree Swallows (Tachycineta bicolor) are secondary cavity nesters, and breeding opportunities are limited by the availability of suitable nest sites (Leffelaar and Robertson 1984, Beasley 1996). This situation creates a large population of nonbreeding male and female floaters (Stutchbury and Robertson 1987). Tree Swallows have one of the highest levels of extrapair paternity among socially monogamous birds (Barber et al. 1996). Dunn et al. (1994) and Kempenaers et al. (1999) attempted to identify extrapair fathers in Tree Swallows using DNA fingerprinting. Despite sampling all locally resident males, the biological fathers of only 21% of the extrapair young were found. Thus, floaters or resident males outside the study area must have fathered extrapair young. During the females’ fertile period, within-pair copulations are very frequent in Tree Swallows (Venier and Robertson 1991). Thus, sperm transferred during an EPC will have to compete with a large number of rival sperm. The aim of this study is to evaluate the potential reproductive role of male floaters in Tree Swallows and to assess whether floater males exhibit adaptations to high levels of sperm competition. We compare the reproductive anatomy and some other characteristics that may indicate quality or condition of floater and resident males. STUDY AREA AND METHODS Field work was carried out during April to June 1997 near the Queen’s University Biological Station (44�34�N, 76�19�W), Chaffeys Locks, Ontario, Canada. We set up a grid of 31 nest boxes in an open field; boxes were put 30 m apart along rows. We caught the settling birds with mist nets or inside nest boxes, banded them with numbered leg bands, and individually marked them using acrylic paint on the wing and/or tail feathers. We determined sex based on plumage characteristics and wing chord (Hussell 1983, Stutchbury and Robertson 1987), by the presence of a cloacal protuberance, and via behavioral observations. For each individual we measured wing and tarsus length using calipers and we estimated muscle score (index from 0 to 3 depending on the amount of muscle tissue covering the sternum) and fat score (index from 0 to 8 depending on the amount of visible subcutaneous fat). We weighed each bird using a Pesola balance and counted the holes in wing and tail feathers caused by feather mites (Acariformes) as a measure of parasite load (see Dunn et al. 1994). For males, we measured the height (h) and diameter (d) of the cloacal protuberance (CP) using calipers. We calculated CP volume as: