Department of Biology, Queen’s University, Kingston

Weak Mate Guarding in Tree Swallows: Ecological Constraint or Female Control?

ANDREW A. CHEK & RALEGH J . ROBERTSON

Ct-IIX, A. A. & ROBERTSON, K. J . 1994: Weak mate guarding in tree swallows: ecological constraint or female control? Ethology 98, 1-13,

Abstract

We re-examined tree swallows (irachycint-ta bicolor) for the presence of the paternity protection tactic of mate guarding using less conservative criteria for its detection than did an earlier study. O u r results are consistent with weak mate guarding, bur may also be explained by the copulatory access hypothesis. T h e latter hypothesi: suggests that the spatio-temporal demands of pair copulation can result in a similar pattern of behaviour to mate guarding. We address two hypotheses advanced previously for the lack of intense mate guarding in this species as compared with other species. These are that female fidelity obviates the need for males to mate guard, and that the risk of nest site usurpation prevents males from guarding. Since tree swallows have one of the highest known races of extra-pair paternity, the first hypothesis is discounted. We find the second hypothesis unlikely after an examination of the species’ ecology, and suggest an alternative hypothesis to account for the lack of intense guarding. In short, we propose that in species such as tree swallows, in which females appear to have a significant degree of interest in, and control over, extra-pair fertilizations, frequent copulation may be a more cost-efficient means of ensuring paternity than is mate guarding.

Corresponding author: Andrcw A. CHEF., Department of Zoology, University of Guelph, Guelph, Ontar io , Canada N1G 2W1.

Introduction

Sperm competition is the contest waged between the sperm of two o r more males over the ovum o r ova of a female (PARKER 1984). Paternity protection tactics are employed by a male to increase his chance of siring the offspring of his mate in the face of sperm competition from other males. In birds the most effective paternity protection tactic is generally considered to be mate guarding (BIKKHEAD & M 0 L L E R 1992). A male bird engaged in mate guarding ostensibly acts as a physical barrier to other males seeking an extra-pair copulation (EPC) with his mate while she is in her fertile period. Hence during the female’s fertile period the

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2 A. A. CHEK & R. J . ROBERTSON

mate-guarding male should spend relatively more time with his mate than he does in periods when she is not fertilizable (BIRKHEAD & M 0 L L E R 1992). Moreover, whenever the.female moves away from her mate to a distance where the chance of her engaging in an EPC is increased, the male is expected to follow the female to lessen this distance and the associated likelihood of EPC.

LEFFELAAR & ROBERTSON (1984) concluded that male tree swallows (Tuchy- cznetu bicolor) did not protect their paternity by mate guarding. They argued that, because female tree swallows did not seem to participate in EPCs, males did not need to guard females. Moreover, LEFFELAAR & ROBERTSON (1984) suggested that defence of the nest site from usurpation precludes intense mate guarding.

An alternative explanation for the absence of intense mate guarding in tree swallows is that the measures used by LEFFELAAR & ROBERTSON (1984) made the detection of mate guarding less likely. Since all measures of mate guarding are made of behaviour exhibited in a female’s fertile, as compared with non-fertile, periods, it follows that the definition of these periods is critical in detecting mate guarding. Female birds are fertile until the day the penultimate egg is laid (JOHNSON 1986) and tree swallows may lay up to seven eggs. LEFFELAAR & ROBERTSON (1984) defined the fertile period of female tree swallows as ending on the fourth day of egg laying. Hence LEFFELAAR & ROBERTSON’S (1984) definition of the fertile period may have been too short, reducing the likelihood of detecting a change in male tactics. In addition, since EPCs in this species are concentrated in the pre-laying period (VENIER et al. 1993), males might limit guarding behaviour to this period. Hence, combining observations from the pre-laying and laying periods, as LEFFELAAR & ROBERTSON (1984) did, may obscure a pattern of male behaviour consistent with mate guarding.

Since following behaviour is the principal means by which males are thought to maintain contact with their mates and prevent EPCs (e.g. BIRKHEAD 1979), the definition of following is then another critical definition in any study of mate guarding. LEFFELAAR & ROEERTSON (1984) looked for males following their mates after every female departure from the nest box, even if during this time the female was simply flying in the vicinity of the next box and foraging. If, after the female’s departure, she remains in sight of her mate, then there would seem to be less chance of an EPC occurring simply because the male is likely to observe any EPC attempt and interfere with it. Hence, a more sensitive measure might be to look for male mate-following behaviour only when the female moved out of sight of the nest site (and the male), in which case she might conceivably copulate with another male.

In this study, we re-examine LEFFELAAR & ROBERTSON’S (1984) tree swallow population for the presence of mate guarding. We hypothesized that their criteria for detecting mate guarding might have been overly conservative and, moreover, that their definition of the female’s fertile period might make the detection of mate guarding less likely. We find that male tree swallows could be considered to mate guard weakly, but that their behaviour can also be explained by GOWATY & PLISSNER’S (1987) copulatory access hypothesis. We then examine the two expla- nations advanced by LEFFELAAR & ROBERTSON (1984) to account for the lack of

Mate Guarding in Tree Swallows 3

intense mate guarding in this species, namely that there is little or no risk of EPC (female fidelity hypothesis), and that a high risk of nest site usurpation precludes intense mate guarding (ecological constraint hypothesis). Finally, we draw upon recent studies of sperm competition in this population of tree swallows and suggest that remarkable female influence over paternity of the brood may be the reason why males adopt frequent copulation, instead of intense mate guarding, as the primary paternity guard.

Methods

Study Species and Site

Tree swallows are small (about 20 g) aerial, insectivorous, passerine birds (ROBERTSON et al. 1992). T h e mating system can be charasterized as monogamous though polygyny does occur at .,bout 3 %a

in ou r population (DUNN & ROBICRTSON 1992). Pairs copulate frequently (mean 51 copulations/clutch; VENIER & ROBERTSON 1991). T h e male hovers over the perched female and usually makes a series of descents that may result in cloac:il contact if the female cooperates. Females easily reject copulations, usually by pressing their tails down and preventing cloacal contact, o r by turning and snapping at the male w h o will then desist. Pairs commence copulating up to 22 d before the first egg is laid, bur the peak in copulation frequency occurs over the 8 d before the first egg (VENIER & ROBERTSON 1991), and drops dramatically on the day that the first egg is laid. Females in ou r population lay between four and seven eggs and incubation commences with the laying of the penultimate egg (personal observations), which in birds coincides with the ovulation of the final ,egg and the end of the fertile period (JOHNSON 1986). Durinl; the nestling period, males and,, fe!males contribute equally KO rhe feeding of the young (LEFFELAAK & ROBERTSON 1986).

W e conducted this s tudy at the Queen's University Biologicat Station (4)."!4'N, 76 "91'W) in south-eastern Ontar io , Canada during May and J u n e 1990 using the population of iree swallows that was used for the studies by, among others, VENIER & ROBERTSON (1991). LIFJELD & ROBERTSON (1992), LIFJELD et al. (1993), V E N I E R et al. 1993, and WHITINGHAM et al. (1993). Accordingly, information on tree swallows derived from these studies is applicable to our findings on mate guarding. T h e swallows used in this study make u p part of the number that occupy 72 nest boxes arranged in grids in three hayfields. Nearest-neighbour distance between nest boxes was 28 m (on the diagonal). This spacing is similar to that of natural nest cavities (RCNDELL 8: ROBERTSON 1989). Average annual occupancy of these nest boxes by tree swallows exceeds 80 YO and was 88 O h in 1990. Unoccupied nest boxes usually result from a pair defending two nest boxes.

At 18 nest boxes we observed the pair for a 15-min interval between 0610 and 1430 h EST each day from 4 May until 3 - 4 d after clutch completion. I n all pairs at least one member was uniquely colour-marked with acrylic paint o n the wing and tail and in most cases both members were marked. Sex was determined from the presence of a cloacal protuberance in males, from brown plumage found only in females in their first breeding season (HUSSELL 1983), from wing length (STUTCI-IBURY & ROBERTSON 1987), o r from position during copulation. During observation periods we used a portable computer to record continuously whether each member of the pair was a t the nest box, flying, o r out of sight of the observer.

/ : . . .

Mate Guarding

Because some females laid earlier than others, the number of days of pre-laying observations for each pair varied (range 6-18). We had observations from 8 d before laying for all but one pair, so we used data from day -8 (day 0 is first-egg-day) to 3-4 d after the last egg had been laid in each clutch.

Like many birds, female tree .iwallows can use sperm stored from previous copulations to fertilize their eggs (LIFJELD & ROBERTSON 1992). The maximum number of days that female tree swallows can store sperm is unknown, so we d o not know exactly how long before the first ovulation a female tree swallow can be regarded as fertilizable. However, since mate guarding is a male tactic, we think it appropriate to consider the female as fertilizable from the date of onset of frequent copulation attempts

4 A. A. CHEK & R. J . ROBERTSON

by males (day -8; VENIER 81 ROBERTSON 1991). The actual fertile period of birds ends with the ovulation of the final egg on the penultimate-egg day (JOHNSON 1986) and this is when we would expect a change in a male’s paternity protection tactics. In tree swallows it may be the appearance of the first, rather than the penultimate, egg that males consider most important from a paternity protection standpoint, because this is when there is a dramatic decrease in copulation frequency (VENIER & ROBERTSON 1991). This decrease may be linked to the fact that observed EPCs are concentrated in the pre-laying period. Because the onset of laying may coincide with a change in tactics of male tree swallows, we divided the fertile period into pre-laying (day -8 to day -1) and laying (day 0 to penultimate-egg day) periods. The post-fertile period stretched from the last day of egg laying to 3 4 d after the last egg and we refer to it as the post-laying period.

We compared male following of females with female following of males. If following behaviour is a manifestation of mate guarding, then males should follow females more than vice versa because males should be the sex that is concerned with maintaining pair contact (BIRKHEAD & M0LLER 1992). For example, if a male followed his mate every time (I00 “/o) she moved away from him, then we might suspect he is guarding her. However, our interpretation might change if we found that the female likewise followed the male every time he moved. More importantly for the detection of mate guarding, male following of their mates should be more intense in the female’s fertile period than in her non-fertile period (BIRKHEAD & M0LLER 1992). If males follow females 100 % of the time even after egg laying is finished, then it is unlikely that it is for the sole purpose of excluding EPCs. We looked for following behaviour whenever both members of the pair were at the nest box and one bird departed and went out of sight of the observer, and, presumably, of the bird remaining at the nest box. As in other studies (MQLLER 1985; GOWATY et al. 1989), we recorded ‘following from’ when the remaining bird departed the nest box within 30 s. In addition, we recorded ‘following to’ whenever both pair members had been out of sight and the second bird to arrive at the nest box did so within 30 s of the first bird’s arrival.

We also tested whether, during their fertile period, females were more likely to move away from males than vice versa. This would be expected if males were attempting to maintain close proximity to their mates (BIRKHEAD 81 M0LLER 1992). Moreover, we would expect that if a male is mate guarding, then he should be less likely to move away from his mate during her fertile period (pre-laying and laying) compared with periods when she is not fertilizable (post-laying).

We assumed that if we could see the male and female, whether flying or perched, then the birds could also monitor each other. Since we could not tell if pairs were in contact when both members were absent, we estimated the proportion of time that the pair was ‘together’ by dividing the time that we could see both members of the pair by the total time that at least one of them was in sight. This is a less conservative measure of pair togetherness than using the amount of time both members of the pair were perched at the nest box as LEFFELAAR & ROBERTSON (1984) did. If male tree swallows were mate guarding, then we expected that they would spend more time in sight of their mate during her fertile period than in her non-fertile period.

We consider the absence of mate guarding as either the lack of any pattern in all presumed mate- guarding behaviour across fertile and non-fertile periods, or the existence of a pattern in matr-guarding behaviour contradictory to the goal of precluding extra-pair ferti!izations. For example, if males are always with their mates in the post-laying period but rarely so in the pre-laying and laying periods, we would consider there to be no mate guarding by males. If some o r all presumed mate-guarding behaviours were more intense in fertile than non-fertile periods, then we would consider males to show behaviour consistent with the tactic of mate guarding. The relative intensity of mate guarding could then be determined by referring to published values for other bird species.

Insemination Window

The ‘insemination window’ (CHENG et al. 1982) refers to the period of perhaps 15 min foilowing each oviposition when the newly ovulated egg is penetrable to sperm (JOHNSON 1986), and when newly introduced sperm (from pair or extra-pair copulations) may have an advantage over sperm stored before ovulation (CHENG et al. 1983). If such a period exists for tree swallows, then mate guarding might be concentrated during this period when EPCs might be potentially most damaging, and relaxed during the rest of the day. Any such pattern would likely be obscured when data from the early morning are combined with those collected during the rest of the day. Because female tree swallows lay between 0620 and 0805 h (VENIER & ROBERTSON 1991), we reasoned that any effect of

Mate Guarding in Tree Swallows 5

the putative insemination window on male mate guarding would likely be concentrated in the period 0615 to 0830 h. Accordingly, we also calculated means for each pair based only on the observations made in the period 0615 to 0830 h.

Data Analysis

For questions involving variation in behaviour across nesting periods, we subjected means for each pair in each nesting period to a one-way repeated-measures analysis of variance. Note that for repeated-measures ANOVA (Friedman’s) a missing value causes all other values for that pair to drop out of the analysis, Thus, for example, i f we never observed a female of a particular pair depart the nest box in the post-laying period while her mate was there, we could not score male following behaviour. Consequently a missing value would result for that period causing observations of male following behaviour for that pair in the pre-laying and laying periods to drop from the analysis. Hence for some analyses the sample size is less than 18 pairs. Most data were either non-normal or heteroscedastic and resisted effective transformation, so we used non-parametric analyses.

Results

Male tree swallows followed females ‘from’ the nest box significantly more often than females followed males (male followed female; X = 25, range 0-100 YO; female followed male; X == 10, range 0-50 %; Wilcoxon T + = 94.5, p <: 0.001, n = 18 pairs). In addition, the tendency for males to follow their mates varied with the nesting period (Friedman x2 corrected for ties = 6.5, p = 0.039, df = 2, n = 6 pairs; Fig. la); males followed their mates more often in the pre-laying period than in subsequent periods. The number of times a female left her mate at the nest box and went out of sight declined after the pre-laying period (pre-laying: X = 0.83, range = 0.25-2.14 departures per observation period; laying: X = 0.2, range 0.14-0.4; post-laying: X = 0.29, range 0.2-0.75; Friedman xZ = 8.33, p = 0.015, df = 2, n = 6) thus affecting the male’s opportunity to display following behaviour. However, since the following analysis considers proportions, rather than absolute values, we do not think that the decline in female departures can be wholly responsible for the decline in male following behaviour.

Overall, males followed their mates ‘to’ the nest box significantly more often than vice versa (male follclwed: X = 35.9, range 0-100 %; female followed: X = 23.2, range 0-50 YO; Wilcoxon T + = 24, p < 0.01, n = 18 pairs). However, in contrast to the trend for following ‘from’, the likelihood of a male following his mate to the nest box declined in the post-laying period rather than the laying period. With small sample sizes for both measures of following behaviour and the fact that the variation across nesting periods in following ‘to’ behaviour is not statistically significant (Friedman x 2 = 2, p = 0.37, df = 2, n = 5 pairs; Fig. Ib) we cannot say whether the apparent contradiction in the two patterns of following behaviour is meaningful. We do note, as have GOWATY et al. (1989), that the following ‘to’ measure may be less reliable than other measures of mate guarding. If, instead of immediately landing (i.e. within 30 s or less) with the female at the nest box, the male remained flying in its vicinity (unbeknownst to the observer), then following to the nest site would be underestimated.

The mate-guarding hypothesis predicts that males should be less likely than females to be responsible for breaking pair contact, or at least that males’ will-

6 A. A. CHEK & R. J . ROBERTSON

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80 -

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20 -

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Nesting period Fig. 1: Box plots represent the X as a horizontal line; 75th and 25th percentiles are upper and lower limits of box. Upper and lower bars define 90th and 10th percentiles. Dots above o r below range bars represent observations that fall outside the 90th and 10th percentiles. (a) Proportion of movements out of sight by one pair member that were followed by the remaining pair member within 30 s. Open bars, male follows female (n = 6 ) ; shaded bars, female follows male (n = 13). Zeroes on abscissa represent 0 % following rather than missing values. (b) Proportion of times one pair member arrived at the nest site within 30 s of the other after both pair members had been absent. Open bars, male

follows female to nest box (n = 5); shaded bars, female follows male to nest box (n = 7)

ingness to break contact should vary inversely with the risk of EPC. We found that males departed and went out of sight, leaving their mate at the box, twice as often (2 = 67.3, range 33.3-87.0 %, n = 17 pairs) as females did (Wilcoxon T + = 163, p < 0.001, n = 17 pairs). However, the likelihood of males leaving their mates alone varied with nesting period (Friedman x2 corrected for ties = 11.63, p = 0.003, df = 2, n = 17 pairs). In the pre-laying period, when other measures of mate guarding peaked, males were less likely to leave their mate behind than they were in subsequent periods (Fig. 2), although within the pre-laying period males still initiated approximately 50 % of departures.

Pairs remained in contact significantly more during the pre-laying period than

Mate Guarding in Tree Swallows 7

0 i 0 1 -

Pre-laying Laying Post-laying Nesting Reriod

Fig. 2: Proportion of all movements resulting in a break of visual contact between pair members that were initiated by the male (n = 17). I n the post-laying period the median is equal to 75th percentile. Note that the proportion of female-initiated movements is equal to 1 - (proportion of male movements)

in the laying and post-laying periods (Friedman x2 = 11.44, p = 0.003, df = 2 , n = 18 pairs; Fig. 3a). In the pre-laying period, when male following was most intense, males were in sight of their mates about half the time. The decrease in pair association from the pre-laying to laying period did not appear to be due to a change in total time the female spent in sight (Friedman x2 = 0.78, p = 0.68, df = 2 , n = 18 pairs). Rather, decreases in male time in sight seemed to be responsible for the pattern of pair association (Friedman x 2 = 8.78, p = 0.012, df = 2, n = 18 pairs; Fig. .3b).

Pairs were in contact more during early morning hours than during the rest of the day. However, in contrast to the predictions of the insemination window hypothesis, there was no significant difference in pair contact over nesting periods when only the early morning hours were considered (Friedman x 2 = 3.82, p = 0.148, df = 2 , n = 11 pairs). Male following of females to and from the nest box during early morning hours could not be statistically assessed over nesting periods due to the number of missing values (see Methods). Finally, the likelihood that a male would depart and leave his mate at the nest box during early morning hours was not different from the pattern shown over the whole day. In sum, a period of intense male mate guarding is not being masked by the combination of data from early morning and from the rest of the day.

Discussion

Do Males Guard Females?

For mate guarding to be demonstrated, males must display behaviour con- sistent with preventing females from engaging in EPCs. More importantly, mate guarding must be more intense in the female's fertile period when an EPC could

8 A. A. CHEP; & R. J . ROBERTSON

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0

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0 Pre-laying Laying Post-laying

Nesting period Fig. 3: (a) Amount of time that the male and female were in sight as a proportion of the time that at least one pair niember was in sight (n = 18). (b) Variation across nesting periods in the proportion of

the trial that the male was in sight (n = 18)

lead to an extra-pair fertilization (BIRKHEAD & M0LLER 1992), or in some part of the fertile period when an EPC is most likely. Since observed EPCs are con- centrated in the pre-laying period (VENIER et al. 1993), mate guarding should be most intense in the pre-laying period when the risk of EPC is greatest. We found that in the pre-laying period, compared with subsequent periods, male tree swallows followed their mates more from the nest site, spent more time in visual contact with their mates, and were less likely to break contact with their mates by leaving them at the nest site. Hence our observations are consistent with the pattern predicted by the mate-guarding hypothesis. Comparison of our results with published values for other species (BIRKHEAD & M 0 L L E R 1992) suggests that if our results truly reflect mate guarding by male tree swallows, then i t is weak guarding. During the peak in ‘guarding’ (pre-laying), tree swallow males initiated more movements away from their mates, followed their mates less, and spent less time in contact with their mates than most of the other birds contained in BIKKHEAD

Mate Guarding in Tree Swailows 9

& M0LLER’s (1992) sampling of the literature. The fact that we employed more liberal definitions of mate guarding than do most studies reinforces the already firm position of tree swallows at the weak end of the mate-guarding continuum.

While consistent with a hypothesis of weak mate guarding, our data are also compatible with GOWATY & PLISSNER’S (1 987) ‘copulatory access hypothesis’. In short, males are expected to spend more time with their mates, and even follow them more, in that part of the breeding season when pair copulations are con- centrated. Variation in m d e behaviour over the course of the breeding season is then a reflection of the mde’s pursuit of pair copulations; any benefit from mate guarding is epiphenomenal. For tree swallows, pair copulations are most common in the pre-laying period (VENIER & ROBERTSON 1991) and this is exactly when we found male tree swallows spent the most time with their mates and followed them the most. Likewise, during the pre-laying period, pairs spent more time together in the early morning and this is the part of the day when copulations are more frequent (VENIER & ROBERTSON 1991). The impact of the pursuit of pair copulations on male behaviour is not surprising if one considers that tree swallows copulate frequently (about 5 1 pair copulations /clutch; VENIER & ROBERTSON 1991). Moreover, the willingness of the female to copulate is unpredictable (VENIEK 1990), which might necessitate the male’s spending significant amounts of time with the female before each copulation occurs.

With the data at hand we cannot distinguish between weak mate guarding and copulatory access as explanations for the behaviour of the male tree swallows that we observed. However, we believe we can state with confidence, that male tree swallows in our population could not be considered to display intense mate guarding relative to other bird species.

Why Don’t Males Guard More Intensely?

In their review of avian sperm competition, BIRKHEAD & M 0 L L E R (1992) emphasize that mate guarding is a more efficient paternity protection tactic than frequent copulation, and indeed, mate guarding does seem to be at least the more common tactic employed as the primary paternity guard in bird species. Hence, whether one views our data as support for the copulatory access hypothesis or for weak mate guarding, it is a legitimate question to ask why male tree swallows d o not mate guard intensely but rather seem to rely on frequent copulation as their primary paternity guard (VENIER & ROBERTSON 1991). LEFFELAAR & ROBERTSON (1984) advanced two hypotheses to account for the perceived ‘absence’ of mate guarding by male tree swallows; the female fidelity hypothesis, and the nest site usurpation hypothesis (our terms). We consider these in turn and then suggest our own hypothesis for the absence of intense mate guarding.

LEFFELAAR & ROBERTSON (1984) suggested that male tree swallows did not mate guard because females did not seem to engage in EPCs and hence there was no need for a paternity protection tactic like mate guarding. However, recent work on the same population that they studied has revealed that EPCs d o occur (MORRILI. & ROBERTSON 1990; VENIER et al. 1993) and that EPCs translate into a high level of extra-pair paternity (38 YO of all nestlings; SO % of all nests, LIFJELD

10 A. A. CHEK & R. J . ROBERTSON

et al. 1993). Clearly, the lack of a risk of cuckoldry does not explain the absence of (intense) mate guarding in tree swallows. In fact, since this level of extra-pair paternity is one of the highest reported for monogamous birds, the lack of intense mate guarding is even more curious.

LEFFELAAR & ROBERTSON (1984) added the idea of an ecological constraint to the reasons why they believed that male tree swallows did not mate guard. They argued that, since tree swallows are secondary cavity nesters unable to excavate their own cavities, the chronic shortage of cavities places a premium on defence of the cavity from potential usurpers. If the risk of cavity usurpation were great enough, then it might easily outweigh the risk and attendant cost of EPCs and thereby account for reduced or absent mate guarding in tree swallows (LEF- FELAAR & ROBERTSON 1984). Although the notion of an ecological constraint is thought to be universally applicable in bird species where mate guarding is absent (BIRKHEAD & MQLLER 1992), we think it is an insufficient explanation for tree swallows for the following reasons.

Despite a floating population of tree swallows at our study site (STUTCHBURY & ROBERTSON 1985), nest box usurpations are rare. Most interactions between pair members and intruders involve simple chasing, although some vigorous fights d o occur, especially between females. We would expect that if usurpation by males were a constant threat, then there would be more instances of elevated physical contests between males and intruders. KREBS (1982) found that risk of territory loss in another secondary-cavity nester, the great tit (Purus major), was not appreciable until a replacement male had ‘owned’ the territory for several hours during the resident’s experimentally enforced absence. Female tree swallows were away from their nest boxes for very short periods of time (pre-laying: .? = 70.2, SE * 9.5 s, laying: X = 131.2, SE * 20.3 s ; this study). It seems unlikely, then, that if a male followed his mate in order to guard her, there would be enough time in which an intruding tree swallow of either sex could develop ownership of the nest site before the return of one or both of the true owners. Significantly, it takes hours for floater tree swallows to occupy and defend excess nest boxes erected during the breeding season (STUTCHBURY & ROBERTSON 1985). Experimentally ‘widowing’ a female tree swallow mimics the risk of cavity usurpation that would be entailed by intense male mate guarding (following) in that the nest site is unguarded whenever the female leaves it. Female tree swallows placed in this position during pre-laying and laying (WHITTINGHAM et al. 1993) were able to retain ownership of their nest box even though foraging needs necessitated their periodic absence from the nest site (L. A. WHIITINGHAM, pers. comm.). This suggests that the risk of nest site usurp- ation is not very high. In sum, it seems unlikely that the risk of nest site usurpation can account for the lack of intense mate guarding.

O u r suggestion for the answer to why tree swallows d o not mate guard intensely involves asking whether female tree swallows’ interest in EPCs, control over the success of copulations in general, and perhaps influence over the process

Mate Guarding in Tree Swallows 11

of fertilization, can combine to make frequent copulation a better paternity protection tactic than mate guarding. Consider the following: tree swallows are one of the few monogamous bird species in which females actively solicit EPCs (personal observations; VENIER et al. 1993), and such female-solicited EPCs account for about 40 Yo OF successful EPCs that are observed (VENIER et al. 1993). Moreover, female tree swallows, like many female birds, have a great deal of control over the success of copulations, rejecting them with apparent impunity (personal observations; VENIER 1990). Control over the success of copulations may allow females a great: deal of control over the translation of copulations into fertilizations. LIFJELD & ROBERTSON (1992) found that female tree swallows experimentally widowed on the first-egg day influenced the paternity share of original and replacement males depending on how long they waited before cop- ulating with the replacement male. Moreover, LIFJELD & ROBERTSON (1992) suggested female tree sw;illows are likely to have post-copulatory influence over fertilization; some eggs were fertilized by the removed, original male even though observed copulatory behaviour predicted that the replacement male should have fertilized these eggs.

If, as suggested above, female tree swallows are unusually interested in engaging in EPCs and are able to manipulate paternity of their brood, either through control over the success of copulations o r some post-copulatory mechan- ism, then what might be the most effective paternity guard for male tree swallows? Given that only one or a few EPCs might be enough to cause a large decrement in the mated-male’s paternity share, only mate guarding at o r near 100 % would be effective in completely preventing extra-pair fertilizations. However, intense mate guarding appears to be energetically expensive, perhaps because following a female closely and remaining constantly vigilant interferes with the mated-male’s foraging for food (MDLLER 1987; BIRKHEAD & MDLLER 1992). If this is so, then no male tree swallow is likely to be able to mate guard 100 % of the time and so exclude every attempt at EPC his mate might make. While the relative energetic demands of frequent copulation and intense mate guarding are not known, it is probably true that the tactic of frequent copulation does not interfere’to the same extent with a male’s foraging as would the vigilance and frequent following of intense mate guarding. Ac:cordingly, a male concentrating on attempting frequent copulations with his mate would incur lower energetic costs whilst also potentially diluting the impact of sperm from EPCs (BIRKHEAD et al. 1987), and perhaps allowing time to pursue ElPCs himself.

No te that we d o not argue that the frequency of copulation is linearly related to paternity share in this species; LIFJELD & ROBERTSON’S (1992) results suggest that this may not be the case. Neither do we suggest that frequent copulation prevents more extra-pair fertilizations than would energetically attainable levels of mate guarding characteristic of other species. We simply suggest that if females are able to manipulate paternity share, then the tactic of frequent copulation may give equivalent paternity ,protection, allow the mated male more opportunity to pursue EPCs, and be less energetically taxing than mate guarding; a combination we would equate with increased efficiency.

12 A. A. CHEK & R. J . ROBERTSON

In conclusion, we suggest that variation in male tree swallows’ behaviour across nesting periods is consistent with weak mate guarding but is also explained by the copulatory access hypothesis. Further, we suggest that the absence of intense mate guarding in this species is unlikely to be due to an ecological constraint, i.e. risk of nest site usurpation. Rather, female determination to engage in EPCs may contribute to making frequent copulation a more efficient paternity protection tactic than intense mate guarding, both energetically and in terms of the male’s opportunities for EPCs. In general, it may be that mate guarding is only effective in species in which females have little interest in EPCs, i.e. they ‘cooperate’ in being guarded by their mates from the advances of other males. In other words, mate guarding may be an effective paternity protection tactic only when it is in the interests of the female as well as the male.

Acknowledgements

We thank Larissa WHITE and Jeremy MITCHELL for field assistance; Queen’s Biological Station for logistic support; members of RJR’s lab and Bob MONTGOMERIE and his lab for useful discussions and statistical advice. We are indebted to Jim BRISKIE, Peter DUNN, Chris NAUGLER and Lisa VENIER for providing comments on an earlier draft of this manuscript, and D r H . Jane BROCKMANN and an anonymous reviewer for constructive criticism. Special thanks to Jan LIFJELD for stimulating alternative ideas about sperm competition. This research was supported by the Natural Sciences and Engineering Research Council of Canada through a scholarship to A. A. CHEK and an operating grant to R. J . ROBERTSON.

Literature Cited

BIRKHEAD, T. R. 1979: Mate guarding in the magpie ficu pica. Anim. Behav. 27, 8 6 6 8 7 4 . _ _ & M0LLER, A. P. 1992: Sperm Competition in Birds: Evolutionary Causes and Consequences.

_ _ , ATKIN, L. & MQLLER, A. P. 1987: Copulation behaviour of birds. Behaviour 101, 101-133. CHENG, K. M . , BURNS, J . T. & MCKINNEY, F. 1982: Forced copulations in captive mallards (Anus

Acad. Press, London.

plutyhynchos): 11. Temporal factors. Anim. Behav. 30, 695-699. _ _ , _ _ & - - 1983: Forced copulation in captive mallards 111: sperm competition. Auk 100,

302-310. DUNN, P. 0. & ROBERTSON, R. J . 1992: Geographic variation in the importance of male parental care

and mating systems in tree swallows. Behav. Ecol. 3, 291-299. GOWATY, P. A. & PLISSNER, J . H. 1987: Association of male and female American robins (Turdus

migrutorius) during the breeding season: paternity assurance by sexual access or mate guarding. Wilson Bull. 99, 5 6 6 2 .

and nest guarding by eastern bluebirds, Siuliu siulis. Anim. Behav. 38, 272-284. _ _ , _ _ & WILLIAMS, T. G. 1989: Behavioural correlates of uncertain parentage: mate guarding

HUSSELL, D. J . 1983: Age and plumage color in female tree swallows. J . Field O m . 54, 312-318. JOHNSON, A. L. 1986: Reproduction in the female. In: Avian Physiology (STURKIE, P. D., ed.).

KREBS, J . R. 1982: Territorial defence in the great tit ( furus major): do residents always win? Behav.

LEFFELAAR, D. & ROBERTSON, R. J . 1984: D o male tree swallows guard their mates? Behav. Ecol.

_ _ & - - 1986: Equality of feeding roles and the maintenance of monogamy in tree swallows.

LIFJELD, J . T., DUNN, P. O., ROBERTSON, R. J . & BOAG, P. T. 1993: Extra-pair paternity in

_ _ & ROBERTSON, R. J . 1992: Female control of extra-pair fertilization in tree swallows. Behav.

Springer-Verl., New York. pp. 104-431.

Ecol. Sociobiol. 11, 185-194.

Sociobiol. 16, 73-79.

Behav. Ecol. Sociobiol. 18, 199-206.

monogamous tree swallows. Anim. Behav. 45, 213-219.

Ecol. Sociobiol. 31, 86-96.

Mate Guarding in Tree Swallows 13

M0LLER. A. P. 1985: Mixed reproductive strategy and mate guarding in a semi-colonial passerine, the swallow Hirundo rusticu. Behav. Ecol. Sociobiol. 17, 401-408.

_ _ 1987: Extent and duration of mate guarding in swallows Hirundo rusticu. Ornis Scand. 18,95- 100.

MORRILL, S. B. & ROBERTSON, R. J . 1990: Occurrence of extra-pair copulation in the tree swallow (Tuchycinetu bicolor). Behav. Ecol. Sociobiol. 26, 291-296.

PARKER, G. A. 1984: Sperm competition and the evolution of animal mating strategies. In: Sperm Competition and the Evolution of Animal Mating Systems (SMITH R. L., ed.). Acad. Press, New York. pp. 2-59.

RENDELL, W. B. & ROBERTSON, R. J . 1989: Nest-site characteristics, reproductive success and cavity availability for tree swallows breeding in natural cavities. Condor 91, 875-885.

ROBERTSON, R. J . , STUTCHBURY, B. S. & COHEN, R. R. 1992: Tree Swallow. The Birds of North America, No. 11 (POOLE, A., STETENHEIM, P. & GILL, F., eds). Acad. Nat. Sci. and Am. Om. Union, Philadelphia/Washington, pp. 28.

STUTCHBURY, B. J . & ROBERTSON, R. J . 1985: Floating populations of female tree swallows. Auk

_ _ & - - 1987: T w o methods of sexing adult tree swallows before they begin breeding. J . Field Om. 58, 236-242.

VENIER, L. A. 1990: Copulation behaviour of tree swallows (Tuchycineta bicolor): paternity assurance in the presence of sperm competition. MS thesis, Queen's Univ., Kingston.

-- , DUNN, P. 0.. LIFJELD, J . T. & ROBERTSON, R. J . 1993: Behavioural patterns of extra-pair copulation in tree swallows. Anim. Behav. 45, 412-415.

_ _ & ROBERTSON, R. J . 1991: Copulation behaviour of the tree swallow, Tuchycineta bicolor: paternity assurance in the presence of sperm competition. Anim. Behav. 42, 939-948.

WHITINGHAM, L. A, , DUNN, F'. 0. & ROBERTSON, R. J . 1993: Confidence of paternity and male parental care: an experimental study in tree swallows. Anim. Behav. 46, 139-147.

102, 651-654.

Received: April 21, 1993

Accepted: May 31, 1994 (J. Brockmunn)