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Paternity and paternal care in the swallow, Hirundo rustica
Anirn. Behav., 1988, 36, 996 1005
Paternity and paternal care in the swallow, Hirundo rustica ANDERS PAPE MOLLER Department of Zoology, Uppsala University, Box 561, S-751 22 Uppsala, Sweden
Abstract. Paternal care in the monogamous swallow, Hirundo rustica, measured in terms of frequency of
feeding of young, was positively related to the certainty of paternity. Male parental care increased with the absolute number of pair copulations and decreased with the absolute and relative number of extra-pair copulations by his mate. Nearly identical results were obtained using either relative or absolute number of male feedings as a measure of the intensity of parental care. Male swallows apparently estimated their certainty of paternity from the interest that neighbouring males were taking in their mates during the fertile period. When the number of extra-pair copulations involving their mates was experimentally increased, males significantly decreased their feeding rates compared with controls. Paternal care was not related to several measures of male quality (body condition, arrival time, mite infection, song rate, or mate guarding rate).
Biparental care is widespread among the generally monogamous birds (Lack 1968). This kind of parental investment where males play an important role could have evolved because (l) males have a relatively high certainty of paternity in monogamous mating systems (Trivers 1972; Alexander 1974), (2) two parents may be necessary to rear the young, i.e. the female cannot do it by herself (Maynard Smith 1977; Perrone & Zaret 1979), and (3) both male and female parents remain close to the hatching offspring because pairs usually breed on territories, and the male, therefore, may as well help look after the young (Williams 1975; Gross & Shine 1981). Even though extra-pair copulations are relatively frequent and taxonomically widespread among birds (Ford 1983; McKinney et al. 1984; Birkhead et al. 1987), the costs of such copulations have only rarely been documented. Costs of extrapair copulations for the female participant may include mate desertion, reduced paternal care, break-up of the pair-bond from one season to another, and increased intra-brood competition for resources because of reduced relatedness between offspring (Hamilton 1964; Trivets 1972; Dawkins 1976; Erickson & Zenone 1976; Grafen & Sibly 1978). Reduced paternal care due to lower certainty of paternity has sometimes been recorded or inferred in some polyandrous or polygynandrous mating systems (Stacey 1979; Joste et al. 1982; Houston & Davies 1985), but not in all cases (Craig & Jamieson 1985). No studies, however, have considered monogamous species of birds although
sperm competition may be very intense in monogamous mating systems (Trivers 1972; Birkhead et al. 1987). In this paper I investigate whether there is a relationship between the intensity of paternal care and the gamete contribution. One prediction is that paternal confidence, and thus paternal care, should be negatively related to the absolute and relative number of extra-pair copulations by the female mate. It is known from domesticated species that the probability of fertilization is proportional to the number of copulations during the fertile period (Martin et al. 1974) and that the viability of sperm decreases with sperm age (Lodge et al. 1971). One would, therefore, predict a positive relationship between the extent of paternal care and the absolute number of pair copulations. These predictions were tested in a mixed observational and experimental study of a marked population of swallows, Hirundo rustica.
METHODS Observational Procedure
I studied colour-ringed and/or dyed (with individual patterns of red, blue and black on their bellies) swallows at Kraghede (57 °12'N, 10°00'E), Denmark, during the breeding seasons 1984-1985 by following 38 broods in two colonies with 18 and 20 pairs (these data were used for the detailed analyses) and 14 broods of solitary pairs. Each individual was watched during only a single breed-
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Moller: Swallow paternity and paternal care
ing season. Brood sizes ranged from two to six nestlings, and each brood was observed daily (see below). Individuals were caught and individually marked and subsequently watched at the breeding sites daily for 2 h between sunrise and 1200 hours during the whole breeding season until the fledglings (which were dyed so individual broods could be identified) disappeared. Several pairs (up to a maximum of eight within a distance of 15 m) were watched simultaneously in the colonies. Each pair was watched for 66-119 days. For the analyses of paternal care during the entire nesting cycle I recorded: (1) the number of feedings per male and female; (2) the number of pair copulations where the male had cloacal contact with his mate; (3) the number of extra-pair copulations where the male had cloacal contact with a female non-mate; (4) the operational sex ratio (mean number of fertile females per male not having a fertile female himself; Emlen & Oring 1977) during the fertile period of the female (estimated to last from 5 days before the start of egg laying until the date when the penultimate egg was laid; Moiler 1985); (5) the number of chases of the female by male non-mates during her fertile period (Moiler 1985); (6) mate guarding in the fertile period measured as the amount of time males spent very close to their mates (percentage of observations at 2-min intervals when a female and her mate were within 5 m of each other; see Moiler 1985); (7) song rate per h by the male in the fertile period of his mate; (8) the date of arrival of males; (9) male wing length, measured to the nearest mm using the flattened wing method (Svensson 1984) when the bird was caught in the evening following arrival; (10) male body weight, measured to the nearest 0.1 g using a Pesola spring balance; (11) the number of haematophagous mites, Ornithonyssus bursa, on the head of the swallow when caught; and (12) the date when the first egg was laid. The operational sex ratio was included in the analyses because males may adjust the intensity of paternal care to the availability of female nonmates; when many females are fertile males may attempt to practise extra-pair copulations rather than feed nestlings. The parasite infection rate was included in the analyses because a high adult infection rate leads to a high nestling infection rate (A. P. Moiler, unpublished data). Nestlings heavily infected with ectoparasites may need more food than other nestlings of a similar age, and feeding
rates of nestlings may thus be affected by the occurrence of parasites. On the basis of these data I calculated: (1) the relative number of extra-pair copulations by the female (number of extra-pair copulations by the female divided by the total number of copulations involving the particular female); (2) the total number of feedings (male plus female feedings); (3) the relative number of male feedings (number of male feedings divided by the total number of feedings); and (4) male body condition index (body weight divided by (wing length)3; I used the cube of wing length in order to obtain a dimensionality similar to body weight). The relative number of male feedings showed considerable variation during the nestling period. Temporal trends were not consistent between pairs, and feeding activity therefore had to be sampled throughout the nestling period as was done in the present study. Body weight and number of insects per bolus did not differ between males and females (t-tests). Feeding rates decrease with increasing colony size in swallows (Mailer 1987b), and the analyses, therefore, were restricted to pairs breeding in the two colonies with 18-20 pairs. Swallows other than the nest owners only rarely provided nestlings with food (Myers & Waller 1977), and as such 'helping' accounted for less than 0.1% of the total number of feedings, it was excluded from the analyses. Intraspecific nest parasitism is relatively common in swallows and might affect the extent of paternal care (Moiler 1987a). However, none of the broods included in the present study was known to be parasitized. To check for diurnal consistency in feeding rates, in 1986 I recorded feeding rates of 20 pairs on a single, randomly chosen day in the morning (from sunrise to 0800 hours), around noon (1100 to 1300 hours), and in the evening (1800 hours to sunset), for 1 h in each period.
Experimental Procedure I experimentally induced extra-pair copulations in the 1986 breeding season by removing males during the fertile period (Moiler 1987d). Ten randomly chosen colonial males whose mates started to lay eggs on day 58+ 11 SD (day 1 = 1 May) were caught at night (0300-0400 hours) in their territory on day - 6.5 + 1-4 SD in their nesting
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cycle (day 0 is the first day after egg laying; clutch size was 4.8 _+0-6 so for this group). They were kept in a cloth bag during the following morning while the activities of their mates were observed for 2 h following sunrise. The males were then released. One control group of 10 males whose mates started to lay eggs on day 59 + 11 sD were caught at night in their territory on day --6.4+ 1.2 SD and were released immediately following capture. Clutch size was 4.9+0.7 so for this group. A second control group of l0 males, whose mates started to lay eggs on day 58+ 17 so, were caught at night (2200-2300 hours) in their territory on day - 6 . 0 + 1.2 SD in the 1983-1984 breeding seasons. These males were detained for the entire night (7-8 h) and subsequently released at dawn. Clutch size for this group was 5"0+0.0 so. All experimental and control pairs bred within the same colony and variation in colony size thus did not affect the results. Birds from the centre of the colony made up a similar fraction of experimental and control pairs. In 1987 ! detained five solitary males for one morning in the pre-laying period, since it was known from earlier studies (Meller 1985) that extra-pair copulations were rare among solitarily breeding pairs. If extra-pair paternity affected the extent of paternal care, detention of solitarily breeding males thus should not affect the intensity of male parental care. These birds started egg laying on day 43 + 9 so and laid a clutch of 4.6 + 0-6 so eggs. I followed the feeding activities of all these experimental and control pairs as described above. I measured the length of the nestling period as the time from hatching of the last egg (checked daily) until fledging of the last nestling (checked daily). Nestling weight was measured to the nearest 0.1 g using a Pesola spring balance when nestlings were aged 15 days. Nestling mortality rate was calculated as number of fledglings dying during the nestling period in relation to the total number of nestlings.
variables were log~-transformed: number of mites, number of copulations, number of extra-pair copulations and operational sex ratio. Values given are m e a n _ s o . Statistics follow Siegel 0956) and Sokal & Rohlf (1981).
RESULTS
Temporal Variation in Feeding Rates Feeding rates around noon tended to be higher than morning and evening feeding rates, but none of the differences was statistically significant (ttest). Diurnal variation in both male, female and total feeding rates and in relative male feeding rate were consistent within pairs (male feeding rate: W=0.84, X2=48.16, df=19, P<0.001; female feeding rate: W=0-81, ~2=46.10, df=19, P<0.001; total feeding rate: W=0-85, Z2=48.29, df=19, P<0.001; relative male feeding rate: W=0.62, X2=35.73, df=19, P<0"02). Morning watches of feeding rates are thus representative of the entire day. All swallows from a particular colony exploited the same feeding areas which were not defended by individuals. Virtually no feeding took place within the territories which covered a few square metres around the nest. Differences in relative and absolute male feeding rates thus were not caused by differential access to feeding grounds.
100
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Statistical Procedure Because many of the potential factors influencing paternal care are interrelated I analysed the data using both product-moment correlation and multiple linear regression. Several variables were not normally distributed and therefore had to be transformed in order to obtain approximately normal distributions. In the analyses the following
I
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20 NO. OF PAIR C O P U L A T I O N S
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Figure 1. Relative number of feedingsby male swallowsin relation to number of pair copulations. Values are mean _+sD for 1-h observation periods for different pairs in the various groups. Numbers in parentheses are number of pairs. Each male was observed for 18-23 days.
Moiler." Swallow paternity and paternal care 100
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Figure 2. Relative number of feedings by male swaUows in relation to number of extra-pair copulations involving the female mate. Values given are mean +_so for l-h observation periods of different pairs in the various groups. Numbers in parentheses are number of pairs. Each male was observed for 18 23 days.
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25 50 75 EPC FRACTION (%)
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Figure 3. Relative number of feedings by male swallows in relation to the percentage of extra-pair copulations out of the total number of copulations involving the female mate. Values are mean + SD for 1-h observation periods for different pairs in the various groups. Numbers in parentheses are number of pairs. Each male was observed for 18-23 days.
Social Dispersion and Feeding Rates Colonial male swallows and solitarily breeding males provided a similar percentage of parental care during the entire nesting cycle (colonial: 50.0 + 11.6%, N = 38; solitary: 50.8 + 8.3%, N = 14, t = 0"01, dr= 50, NS). The variation in paternal care between pairs was, however, much larger among colonial than among solitarily breeding swallows (F= 10.82, dr=37, 13, P<0.001).
Copulations and Feeding Rates M a n y factors may influence feeding rates in birds including brood size, food availability, time of season, time of day, body size of parent and contribution of the male (Davies 1986; H o w e 1979; Joste et al. 1982; Wittenberger 1982; McGillivray 1984). Analyses of the relative rather than the absolute number of male feedings should control for all of these factors except from the contribution of the male. I have thus concentrated on such analyses, but results obtained from analyses of absolute male feeding rates are very similar, as shown below. The relative number of male feedings for each pair increased with the number of pair copulations seen during observations (r = 0'60, t = 4-50, dr= 36, P<0"001; Fig. 1). The absolute number of male feedings also increased with the number of pair copulations (r=0.44, t=2-94, d r = 3 6 , P < 0 . 0 1 ) .
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Figure 4. Relative number of feedings by male swallows in relation to number of chases involving the female mate. Values are mean + SD for 1-h observation periods for different pairs in the various groups. Numbers in parentheses are number of pairs. Each male was observed for 18-23 days.
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Table 1. Relative number of male feedings during the nestling period in relation to various variables in a multiple linear regression analysis (N= 38) Independent variable
Regression coefficient 4- SE
0.05___0.02 Absolute number of pair copulations -0.13___0.06 Absolute number of extra-pair copulations by female -0.29+0.13 Relative number of extra-pair copulations by female -- 0-004 -+ 0.002 Number of chases of female -- 0.003 4- 0.002 Arrival date of male --0"21 x 10 4-+8"16 x 10-4 Egg-laying date of female Male wing length 0.00 +0.00 Male body weight -- 0-03 -+0.01 0.17 x 10-7_ 1.44 x 10 -7 Male body condition index Male mite infection - - 0"006 + 0' 120 Male song rate 0.003 4- 0.002 Mate guarding 0.06__+0.10 Operational sex ratio 0.03 + 0.03 --0-31x10 4__+0.62x10 -4 Total number of feedings
The relative n u m b e r o f male feedings decreased with the n u m b e r of extra-pair copulations involving the m a t e (r = - 0-68, t = 5"56, df= 36, P < 0"001; Fig. 2). A similar relation was f o u n d for absolute n u m b e r o f male feedings ( r = - 0 . 5 6 , t=4'06, df= 36, P < 0"001). W h e n extra-pair copulations m a d e up a large percentage o f the total n u m b e r o f copulations, male swallows tended to feed nestlings relatively a n d absolutely less frequently t h a n w h e n extra-pair c o p u l a t i o n s h a d n o t occurred (relative n u m b e r o f male feedings: r = - 0 . 3 7 , t=2'39, df= 36, P < 0-05, Fig. 3; absolute n u m b e r o f male feedings: r = - 0 . 3 4 , t=2.19, df=36, P<0-05). Male swallows c a n n o t record extra-pair copula-
P <0.01 <0.05 <0.05 < 0.01 NS NS NS < 0.05 NS NS MS NS NS NS
tions directly, because, if present, they interfere to prevent such c o p u l a t i o n s (Moiler 1985). They may, however, record the interest t h a t n e i g h b o u r i n g males are taking in their mates from the frequency o f n e i g h b o u r s chasing their females. Some o f these chases lead to extra-pair copulations (Moiler 1985). Relative a n d absolute frequency o f male feedings decreased as the frequency of female chases by n e i g h b o u r i n g males increased (relative male feedings: r = - 0 . 7 0 , t=5.88, df=36, P < 0 . 0 0 1 , Fig. 4; absolute male feedings: r = - 0 " 7 0 , t = 5 ' 8 8 , d f = 36, P < 0 " 0 0 1 ) . Since the variables are interrelated, the results were checked in a multiple linear regression. T h e
II. Total number of male feedings during the nestling period in relation to various variables in a multiple linear regression analysis ( N = 38) Table
Independent variable
Regression coefficient_+ sE
Absolute number of pair copulations 50.79 _+20.59 Absolute number of extra-pair copulations by female -- 147.07_+62.28 Relative number of extra-pair copulations by female --3-04__+ 1.28 --3.84___ 1.52 Number of chases of female 0.45 + 0.79 Arrival date of male -- 17.28+ 12'44 Male wing length 83"64 __+65"90 Male body weight -- 13 257"62--+7920"86 Male body condition index 2"76_+ 12'35 Male mite infection 3"00 + 1"95 Male song rate 2"66 -- 1"69 Mate guarding --35'61 +28'45 Operational sex ratio Total number of feedings 0-45 -+0"06
P < 0.05 <0-05 <0.05 <0-05 MS NS NS NS NS MS NS MS < 0"001
Moiler: Swallow paternity and paternal care
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Table Ill. Feeding rates of pairs with an increased number of female extra-pair copulations (experimental colonial), of experimental solitary pairs and of control pairs (controls)
Feeding rate Male feeding rate per h Female feedingrate per h Total feeding rate per h Male feedings (%) N
Colonial Solitary experimentals experimentals 5.2 + 1.7 8.6+ 1.3 13.8+2.6 36.3 +__7.2 10
12-3___3.4 10.8___2.2 23.1 +5.4 53-1 ___8.5 5
Colonial controls caught and released at night
Colonial controls caught and detained during night
11.4__+1.9 12.7___2.7 24.1 __+4-3 47.8 ___3.3 10
10.7 + 2.9 12.2+6.0 22.9+8.7 48.6__.8.2 10
Values are mean + so. All differencesbetween colonial experimental and other groups are significant (Mann-Whitney U-test, P < 0.001) whereas differences between other groups are non-significant.
relative number of male feedings was significantly related to the different variables (multiple r 2---0-56, N=38, F=2"37, df=14, 23, P<0"05, Table I). Male swallows fed young at a higher rate when pair copulations were more frequent and when extrapair copulations were absolutely and relatively infrequent (Table I). Male parental care also decreased with an increasing number of chases of the female by alien males (Table I). The absolute number of male feedings during the nestling period was more closely related to the variables than was the relative number of male feedings (multiple r2=0-88, N = 3 8 , F=12-22, df= 14, 23, P<0.001, Table II). Again, the same variables were of importance; males fed young more often when having copulated more with their mates, when extra-pair copulations were few, and when the relative number of extra-pair copulations was small. Male swallows also provided relatively little parental care if the mate had been chased frequently by male neighbours during her fertile period (Table II). The male contribution of feedings was strongly positively correlated with the total number of feedings (Table II), and swallows thus seemed to adjust their parental care in relation to the contribution of the mate. The operational sex ratio during the fertile period of the female mate affected neither the male fraction of feedings nor the absolute number of male feedings (Tables I and II). Males arriving early in spring, being in better condition, spending much time singing and guarding their mates, and carrying fewer parasitic mites should be of a higher quality than other males. None of these variables, however, was significantly related to the intensity of later paternal care (Tables I and II).
'Experimental' Extra-pair Copulations and Feeding Rates Experimental colonial females experienced 0-7+0-5 (N=10) extra-pair copulations per h whereas control females experienced no extra-pair copulations ( U = 10, N~ = 10, N2= 10, P=0-002, M~ller 1987c). Experimental solitary females did not experience any extra-pair copulations. Only a minor percentage of females (18%) have been recorded as participating in extra-pair copulations, and the absence of extra-pair copulations in the control groups did not deviate from expectation (0 versus 1.8 expected, binomial test, P=0.13). Experimental removal of colonial male swallows during the fertile period of their mates significantly reduced the relative and absolute number of male feedings during the nestling period (Table III). Female mates also decreased their feeding rates among experimental colonial pairs relative to the feeding rates of control females. The reduction of the feeding rate in the females, however, was smaller than the male reduction leading to a decrease in the relative male contribution in experimental colonial pairs (Table III). The experimental colonial group differed from both control groups in the extent of parental care whereas the two control groups did not differ from each other (Table III). Experimental solitary pairs did not deviate from any of the control groups in the extent of parental care (Table III). The length of the nestling periods were similar in the four groups (experimental colonial: 21.2_+ 1.0 days, experimental solitary: 20.8_+0.8 days, control 1:20-8_+0"6 days, control 2:20-8+0.6 days, Mann-Whitney U-test, all MS). Mean nestling weight per brood on day 15 in the nestling period
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was also similar in the four groups (experimental colonial: 20-1 + 1-9 g, experimental solitary: 22.2+1-2 g, control l: 21.3+_1.1 g, control 2: 21-0+_1.3 g, Mann-Whitney U-test, all NS). Nestling mortality rate per brood was much larger in the experimental colonial than in any of the other groups (experimental colonial: 27_+30%, experimental solitary: 0 + 0%, control 1: 0_+ 0%, control 2: 2_+6%, Mann-Whitney U-test, U=7-5, P = 0.002, U = 10, P=0-002, U = 14, P<0.02, respectively). Nestling mortality was apparently caused by starvation.
DISCUSSION Paternal Care
My results show that male swallows provided significantly more parental care if they had copulated frequently with their mates during their fertile period and if the absolute and relative number of extra-pair copulations were few. An experimental increase in the number of extra-pair copulations experienced by the female mate and, thus, probably in the uncertainty of paternity, led to a decrease in the male contribution of feedings. The experimental treatment could have influenced the results as experimental males had to be detained longer than controls in order to obtain the difference in the frequency of extra-pair copulations. A long-lasting disturbance of experimental males may cause a reduction in future paternal care, and a larger reduction in experimental male compared with experimental female provisioning of nestlings. However, all-night detention of males in a previous year did not lead to a reduction in paternal care, and so the experimental results were probably due to differences in activities in the morning rather than differences in the extent of disturbance. The lack of reduction in the amount of parental care in experimental solitary swallows also suggests that the results are not an effect of the experimental procedure. Experimental colonial and control pairs bred at the same time of the season, were caught at a similar time in their nesting cycle and laid clutches of a similar size. Experimental colonial and control males nested in the same colonies, and effects of colony size upon food abundance or sexual activity of individuals were thus similar for all individuals. The reduction in the amount of parental care led to fledging of fewer nestlings although these nestlings fledged at a similar age and had a similar body
weight as those of the control groups. Males thus apparently provided food to the brood at a lower rate when uncertain of their paternity. This interpretation rests upon the assumption that extra-pair copulations with a certain probability can lead to fertilization. This appears to be true for the swallow according to parent-offspring regressions of tarsus length (Meller 1987a). An alternative explanation for variation in the relative contribution of the sexes to parental care is that males that are of a higher quality than their mates can afford to feed nestlings relatively little. This so-called differential-allocation hypothesis (Burley 1986) postulates that mates of attractive individuals will have to pay for this quality by making a relatively high parental investment. However, it is difficult to imagine that quality differences between mates should be greater or more common among colonial than solitarily breeding swallow pairs, as would be required to explain the larger variance in paternal care in colonies than among solitary pairs. Food abundance per individual swallow decreases with colony size, and swallows breeding in colonies thus provide less food to their nestlings per time unit than solitary breeders (Moiler 1987b). The larger variance in the extent of paternal care among colonial than solitarily breeding swallows thus cannot be attributed to the effect of food abundance. A third explanation might be that males provide little parental care because they spend time seeking extra-pair copulations. However, this is unlikely because chases and extra-pair copulations are relatively infrequent, especially during the nestling period (Moiler 1985), and occupy at most a few per cent of the time budget of breeding swallows. Sexual behaviour of swallows changes with age and young inexperienced females and old experienced males especially participate in chases and extra-pair copulations (Meller 1985). The breeding experience of pair members was positively related (A. P. Moiler, unpublished data). Experienced breeders were not spatially concentrated, e.g. in the centre of colonies (A. P. Moller, unpublished data), and the correlation between extra-pair copulations and male feeding rates therefore cannot be explained by a correlation of both factors with experience. The change in female parental care seen in the present study was expected from a theoretical point of view. If the cost of cooperative behaviour (e.g. parental care) increases for one but not another
Moiler: Swallow paternity and paternal care
member of a cooperative unit, then the individual with an increased cost is predicted to decrease its contribution, too, in order to maximize its own inclusive fitness (Chase 1980). The reduction in the amount of parental care due to the non-cooperative behaviour of the male swallow was to some extent compensated by the female mate. Experimental colonial males contributed 46-49% of the feeding rate of the male control groups whereas the experimental colonial females compensated for the low male feeding rate by contributing 68-70% of the feeding rate of the female control groups. This differential sexual willingness to provide cooperative behaviour may arise from a female-biased certainty of having contributed genetically to offspring in the nest. How can male swallows estimate their certainty of paternity? Males never witness extra-pair copulation attempts without interfering (M~ller 1985). However, males may estimate the interest that other males are taking in their mates from the number of chases. Paternal care was in fact negatively related to the number of chases of their mate by male neighbours (Tables I, II and III), and many of these chases were witnessed by the mates of the chased females. This correlation was not caused by males chasing away intruding males during the nestling period and thus spending little time feeding their own nestlings; chases were almost absent during the nestling period (see also Moiler 1985). Male swallows may also have used chases as a cue to their certainty of paternity in the experimental situation because neighbouring males frequently chased experimental colonial females after the release of experimental colonial male swallows (Moiler 1987d).
Female Costs and Benefits of Extra-pair Copulations Why do females engage in extra-pair copulations if as a result they reduce their mate's contribution to parental care? My data showed that female parental care was inversely related to male parental care, and parents thus appeared to adjust their contribution to that of their mate, perhaps as a response to the intensity of the begging calls of the nestlings. Although female swallows do not actively seek extra-pair copulations, they do not try to avoid all of them. Many extra-pair copulation attempts are refused, apparently because of the quality of the male involved (A. P. Moiler, unpub-
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lished data), but others are accepted without any resistance even by the same female (Mailer 1985, unpublished data). The benefits of extra-pair copulations have to exceed or at least equal the costs for the female to participate willingly. One suggestion is that females may benefit from copulating with already mated males of superior quality (see Moller 1985). A second is that females obtain 'helpers' to feed their young by engaging in extra-pair copulations. This, however, is not the case in the swallow. A third reason may be to avoid infanticide (Crook & Shields 1985). But females never copulated with unmated males which are most likely to practise infanticide even though such males attempted extra-pair copulations (A. P. Moiler, unpublished data). Fourth, females may benefit from extra-pair copulations by improving their chances of laying fertile eggs, e.g. if their present mate proves to be infertile. This is highly unlikely since totally infertile clutches were very rare both among colonially and solitarily breeding swallows ( N = 1083 clutches. A. P. Moller, unpublished data). Another suggestion is that males whose mates indulge in extra-pair copulations anyway would not provide much parental care. This last possibility can be excluded in this case since the pairs were assigned randomly to the experimental and the control groups. The greater variance in paternal care among colonial than solitarily breeding swallows is in agreement with the interpretation that the certainty of paternity influences male parental care. In contrast to colonial birds, solitarily breeding females never experience extra-pair copulations (Moller 1985), and only colonial females had mates that provided little food for the young. In conclusion, females may benefit from extra-pair copulations because of the 'good' genes provided by extra-pair copulation partners. One might think that attributes of male quality other than copulation activity may influence the amount of paternal care. However, it was not significantly related to measures of male quality such as body condition, time of arrival in spring, song activity, mite infection, or mate guarding. This suggests that the amount of parental care given by a male is primarily determined by his certainty of paternity, as estimated by the copulation and extra-pair copulation activity of the female and to a much smaller extent, if at all, by other male attributes. If the results presented here are general for monogamous bird species, this would have con-
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siderable i m p o r t a n c e in several fields o f behavioural ecology a n d e v o l u t i o n a r y biology. Males may estimate their certainty o f paternity f r o m intrusion rates into their territories. It m a y thus be unjustified to c o m p a r e the paternal care given by individuals w i t h o u t correcting for differences in extra-pair copulation frequency a n d the concomitant differences in paternity certainty. Paternal care c a n n o t be used as a measure o f p a r e n t a l investment (e.g. Howe 1979; W i t t e n b e r g e r 1982; McGillivray 1984) w i t h o u t taking into a c c o u n t the influence o f differences in the certainty o f paternity. Increased p a r e n t a l investment with age, which has been claimed to be due to changes in the residual reproductive value (Pugesek 1981), m a y in fact be due to age-related changes in the certainty o f paternity.
ACKNOWLEDGMENTS T. R. Birkhead, A. L u n d b e r g a n d S. U l f s t r a n d all provided constructive criticism of earlier drafts o f this paper. T h e research was s u p p o r t e d by a g r a n t from the Swedish N a t u r a l Science Research C o u n cil.
REFERENCES Alexander, R. D. 1974. The evolution of social behavior. ,4. Rev. Ecol. Syst., 4, 325 383. Birkhead, T. R., Atkin, L. & Moiler, A. P. 1987. Copulation behaviour of birds. Behaviour, 101, 101 138. Burley, N. 1986. Sexual selection for aesthetic traits in species with biparental care. Am. Nat., 127, 415-445. Chase, I. D. 1980. Cooperative and noncooperative behavior in animals. Am. Nat., 115, 827-857. Craig, J. L. & Jamieson, I. G. 1985. The relationship between presumed gamete contribution and parental investment in a communally breeding bird. Behav. Ecol. Sociobiol., 17, 207-21 I. Crook, J. R. & Shields, W. M. 1985. Sexually selected infanticide in adult male barn swallows. Anim. Behav., 33, 754-761. Davies, N. B. 1986. Reproductive success of dunnocks, Prunella modularis, in a variable mating system. I. Factors influencing provisioning rate, nestling weight and fledging success, J. Anita. Ecol., 55, 123-138. Dawkins, R. 1976. The Selfish Gene. Oxford: Oxford University Press. Emlen, S. T. & Oring, L. W. 1977. Ecology, sexual selection and the evolution of mating systems. Science, N.Y., 197, 215-223. Eriekson, C. J. & Zenone, P. G. 1976. Courtship differences in male ring doves: avoidance of cuckoldry? Science, N.Y., 191, 1353 1354.
Ford, N. L. 1983. Variation in mate fidelity in monogamous birds. Curt. Ornithol., l, 329-356. Grafen, A. & Sibly, R. 1978. A model of mate desertion. Anita. Behav., 26, 645-652. Gross, M. R. & Shine, R. 1981. Parental care and mode of fertilization in ectothermic vertebrates. Evolution, 35, 775-793. Hamilton, W. D. 1964. The genetieal evolution of social behavior. J. theor. Biol., 7, 1-52. Houston, A. I. & Davies, N. B. 1985. The evolution of cooperation and life history in the dunnock Prunella modularis. In: BehaviouralEcology (Ed. by R. M. Sibly & R. H. Smith), pp. 471~487. Oxford: Blackwell Scientific Publications. Howe, H. F. 1979. Evolutionary aspects of parental care in the common grackle, Quiscalus quiscula L. Evolution, 33, 41-51. Joste, N. E., Koenig, W. D., M u m m e , R. L. & Pitelka, F.A. 1982. Intragroup dynamics of a cooperative breeder: an analysis of reproductive roles in the acorn woodpecker. Behav. Ecol. SociobioL, 11, 195-201. Lack, D. 1968. Ecological Adaptations for Breeding in Birds. London: Methuen. Lodge, J. R., Fechheimer, N. S. & Jaap, R. G. 1971. The relationship of in vivo sperm storage interval to fertility and embryonic survival in the chicken. Biol. Reprod., 5, 252 257. McGillivray, W. B. 1984. Nestling feeding rates and body size of adult house sparrows. Can. J. Zool., 62, 381385. McKinney, F., Cheng, K. M. & Bruggers, D. 1984. Sperm competition in apparently monogamous birds. In: Sperm Competition and the Evolution o f Animal Mating Systems (Ed. R. L. Smith), pp. 523-545. Orlando: Academic Press. Martin, P. A., Reimers, T. J., Lodge, J. R. & Dziuk, P. J. 1974. The effect of ratios and numbers of spermatozoa mixed from two males on the production of offspring. J. Reprod. Fert., 39, 251 258. Maynard Smith, J. 1977. Parental investment: a prospective analysis. Anita. Behav., 25, 1-9. Moller, A. P. 1985. Mixed reproductive strategy and mate guarding in a semi-colonial passerine, the swallow Hirundo rustica. Behav. Ecol. Sociobiol., 17, 401 ~408. Moller, A. P. 1987a. Behavioural aspects of sperm competition in swallows Hirundo rustiea. Behaviour, 100, 92-104. Moller, A. P. 1987b. Intraspecific nest parasititism and anti-parasite behaviour in swallows, Hirundo rustica. Anita. Behav., 35, 247-254. Moller, A. P. 1987c. Advantages and disadvantages of coloniality in the swallow, Hirundo rustica. AnOn. Behav., 35, 819-832. Moiler, A. P. 1987d. Mate guarding in the swallow Hirundo rustica: an experimental study. Behav. Ecol. Sociobiol., 2I, 119-123. Myers, G. R. & Waller, D. W. 1977. Helpers at the nest in barn swallows. Auk, 94, 596. Perrone, M. & Zaret, T. M. 1979. Parental care patterns in fishes. Am. Nat., 113, 351-361. Pugesek, B. H. 1981. Increased reproductive effort with age in the California gull (Larus californicus). Science, N.Y., 212, 822-823.
Moiler. Swallow paternity and paternal care Siegel, S. 1956. Nonparametric Statistics for the Behavioral Sciences. Tokyo: McGraw-Hill Kogakusha. Sokal, R. R. & Rohlf, F. J. 1981. Biometry. San Francisco: Freeman. Stacey, P. B. 1979. Kinship, promiscuity and communal breeding in the acorn woodpecker. Behav. Ecol. Sociobiol., 6, 53 66. Svensson, L. 1984. Identification Guide to European Passerines. Stockholm: Privately published. Trivers, R. L. 1972. Parental investment and sexual selection. In: Sexual Selection and the Descent of Man,
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1871-1971 (Ed. by B. Campbell), pp. 136-179. Chicago: Aldine Press. Williams, G. C. 1975. Sex and Evolution. Princeton: Princeton University Press. Wittenberger, J. F. 1982. Factors affecting how male and female bobolinks apportion parental investments. Condor, 84, 22-39. (Received 11 February 1987; revised 24 September 1987; MS. number: 2963)
Paternity and paternal care in the swallow, Hirundo rustica ANDERS PAPE MOLLER Department of Zoology, Uppsala University, Box 561, S-751 22 Uppsala, Sweden
Abstract. Paternal care in the monogamous swallow, Hirundo rustica, measured in terms of frequency of
feeding of young, was positively related to the certainty of paternity. Male parental care increased with the absolute number of pair copulations and decreased with the absolute and relative number of extra-pair copulations by his mate. Nearly identical results were obtained using either relative or absolute number of male feedings as a measure of the intensity of parental care. Male swallows apparently estimated their certainty of paternity from the interest that neighbouring males were taking in their mates during the fertile period. When the number of extra-pair copulations involving their mates was experimentally increased, males significantly decreased their feeding rates compared with controls. Paternal care was not related to several measures of male quality (body condition, arrival time, mite infection, song rate, or mate guarding rate).
Biparental care is widespread among the generally monogamous birds (Lack 1968). This kind of parental investment where males play an important role could have evolved because (l) males have a relatively high certainty of paternity in monogamous mating systems (Trivers 1972; Alexander 1974), (2) two parents may be necessary to rear the young, i.e. the female cannot do it by herself (Maynard Smith 1977; Perrone & Zaret 1979), and (3) both male and female parents remain close to the hatching offspring because pairs usually breed on territories, and the male, therefore, may as well help look after the young (Williams 1975; Gross & Shine 1981). Even though extra-pair copulations are relatively frequent and taxonomically widespread among birds (Ford 1983; McKinney et al. 1984; Birkhead et al. 1987), the costs of such copulations have only rarely been documented. Costs of extrapair copulations for the female participant may include mate desertion, reduced paternal care, break-up of the pair-bond from one season to another, and increased intra-brood competition for resources because of reduced relatedness between offspring (Hamilton 1964; Trivets 1972; Dawkins 1976; Erickson & Zenone 1976; Grafen & Sibly 1978). Reduced paternal care due to lower certainty of paternity has sometimes been recorded or inferred in some polyandrous or polygynandrous mating systems (Stacey 1979; Joste et al. 1982; Houston & Davies 1985), but not in all cases (Craig & Jamieson 1985). No studies, however, have considered monogamous species of birds although
sperm competition may be very intense in monogamous mating systems (Trivers 1972; Birkhead et al. 1987). In this paper I investigate whether there is a relationship between the intensity of paternal care and the gamete contribution. One prediction is that paternal confidence, and thus paternal care, should be negatively related to the absolute and relative number of extra-pair copulations by the female mate. It is known from domesticated species that the probability of fertilization is proportional to the number of copulations during the fertile period (Martin et al. 1974) and that the viability of sperm decreases with sperm age (Lodge et al. 1971). One would, therefore, predict a positive relationship between the extent of paternal care and the absolute number of pair copulations. These predictions were tested in a mixed observational and experimental study of a marked population of swallows, Hirundo rustica.
METHODS Observational Procedure
I studied colour-ringed and/or dyed (with individual patterns of red, blue and black on their bellies) swallows at Kraghede (57 °12'N, 10°00'E), Denmark, during the breeding seasons 1984-1985 by following 38 broods in two colonies with 18 and 20 pairs (these data were used for the detailed analyses) and 14 broods of solitary pairs. Each individual was watched during only a single breed-
996
997
Moller: Swallow paternity and paternal care
ing season. Brood sizes ranged from two to six nestlings, and each brood was observed daily (see below). Individuals were caught and individually marked and subsequently watched at the breeding sites daily for 2 h between sunrise and 1200 hours during the whole breeding season until the fledglings (which were dyed so individual broods could be identified) disappeared. Several pairs (up to a maximum of eight within a distance of 15 m) were watched simultaneously in the colonies. Each pair was watched for 66-119 days. For the analyses of paternal care during the entire nesting cycle I recorded: (1) the number of feedings per male and female; (2) the number of pair copulations where the male had cloacal contact with his mate; (3) the number of extra-pair copulations where the male had cloacal contact with a female non-mate; (4) the operational sex ratio (mean number of fertile females per male not having a fertile female himself; Emlen & Oring 1977) during the fertile period of the female (estimated to last from 5 days before the start of egg laying until the date when the penultimate egg was laid; Moiler 1985); (5) the number of chases of the female by male non-mates during her fertile period (Moiler 1985); (6) mate guarding in the fertile period measured as the amount of time males spent very close to their mates (percentage of observations at 2-min intervals when a female and her mate were within 5 m of each other; see Moiler 1985); (7) song rate per h by the male in the fertile period of his mate; (8) the date of arrival of males; (9) male wing length, measured to the nearest mm using the flattened wing method (Svensson 1984) when the bird was caught in the evening following arrival; (10) male body weight, measured to the nearest 0.1 g using a Pesola spring balance; (11) the number of haematophagous mites, Ornithonyssus bursa, on the head of the swallow when caught; and (12) the date when the first egg was laid. The operational sex ratio was included in the analyses because males may adjust the intensity of paternal care to the availability of female nonmates; when many females are fertile males may attempt to practise extra-pair copulations rather than feed nestlings. The parasite infection rate was included in the analyses because a high adult infection rate leads to a high nestling infection rate (A. P. Moiler, unpublished data). Nestlings heavily infected with ectoparasites may need more food than other nestlings of a similar age, and feeding
rates of nestlings may thus be affected by the occurrence of parasites. On the basis of these data I calculated: (1) the relative number of extra-pair copulations by the female (number of extra-pair copulations by the female divided by the total number of copulations involving the particular female); (2) the total number of feedings (male plus female feedings); (3) the relative number of male feedings (number of male feedings divided by the total number of feedings); and (4) male body condition index (body weight divided by (wing length)3; I used the cube of wing length in order to obtain a dimensionality similar to body weight). The relative number of male feedings showed considerable variation during the nestling period. Temporal trends were not consistent between pairs, and feeding activity therefore had to be sampled throughout the nestling period as was done in the present study. Body weight and number of insects per bolus did not differ between males and females (t-tests). Feeding rates decrease with increasing colony size in swallows (Mailer 1987b), and the analyses, therefore, were restricted to pairs breeding in the two colonies with 18-20 pairs. Swallows other than the nest owners only rarely provided nestlings with food (Myers & Waller 1977), and as such 'helping' accounted for less than 0.1% of the total number of feedings, it was excluded from the analyses. Intraspecific nest parasitism is relatively common in swallows and might affect the extent of paternal care (Moiler 1987a). However, none of the broods included in the present study was known to be parasitized. To check for diurnal consistency in feeding rates, in 1986 I recorded feeding rates of 20 pairs on a single, randomly chosen day in the morning (from sunrise to 0800 hours), around noon (1100 to 1300 hours), and in the evening (1800 hours to sunset), for 1 h in each period.
Experimental Procedure I experimentally induced extra-pair copulations in the 1986 breeding season by removing males during the fertile period (Moiler 1987d). Ten randomly chosen colonial males whose mates started to lay eggs on day 58+ 11 SD (day 1 = 1 May) were caught at night (0300-0400 hours) in their territory on day - 6.5 + 1-4 SD in their nesting
998
Animal Behaviour, 36, 4
cycle (day 0 is the first day after egg laying; clutch size was 4.8 _+0-6 so for this group). They were kept in a cloth bag during the following morning while the activities of their mates were observed for 2 h following sunrise. The males were then released. One control group of 10 males whose mates started to lay eggs on day 59 + 11 sD were caught at night in their territory on day --6.4+ 1.2 SD and were released immediately following capture. Clutch size was 4.9+0.7 so for this group. A second control group of l0 males, whose mates started to lay eggs on day 58+ 17 so, were caught at night (2200-2300 hours) in their territory on day - 6 . 0 + 1.2 SD in the 1983-1984 breeding seasons. These males were detained for the entire night (7-8 h) and subsequently released at dawn. Clutch size for this group was 5"0+0.0 so. All experimental and control pairs bred within the same colony and variation in colony size thus did not affect the results. Birds from the centre of the colony made up a similar fraction of experimental and control pairs. In 1987 ! detained five solitary males for one morning in the pre-laying period, since it was known from earlier studies (Meller 1985) that extra-pair copulations were rare among solitarily breeding pairs. If extra-pair paternity affected the extent of paternal care, detention of solitarily breeding males thus should not affect the intensity of male parental care. These birds started egg laying on day 43 + 9 so and laid a clutch of 4.6 + 0-6 so eggs. I followed the feeding activities of all these experimental and control pairs as described above. I measured the length of the nestling period as the time from hatching of the last egg (checked daily) until fledging of the last nestling (checked daily). Nestling weight was measured to the nearest 0.1 g using a Pesola spring balance when nestlings were aged 15 days. Nestling mortality rate was calculated as number of fledglings dying during the nestling period in relation to the total number of nestlings.
variables were log~-transformed: number of mites, number of copulations, number of extra-pair copulations and operational sex ratio. Values given are m e a n _ s o . Statistics follow Siegel 0956) and Sokal & Rohlf (1981).
RESULTS
Temporal Variation in Feeding Rates Feeding rates around noon tended to be higher than morning and evening feeding rates, but none of the differences was statistically significant (ttest). Diurnal variation in both male, female and total feeding rates and in relative male feeding rate were consistent within pairs (male feeding rate: W=0.84, X2=48.16, df=19, P<0.001; female feeding rate: W=0-81, ~2=46.10, df=19, P<0.001; total feeding rate: W=0-85, Z2=48.29, df=19, P<0.001; relative male feeding rate: W=0.62, X2=35.73, df=19, P<0"02). Morning watches of feeding rates are thus representative of the entire day. All swallows from a particular colony exploited the same feeding areas which were not defended by individuals. Virtually no feeding took place within the territories which covered a few square metres around the nest. Differences in relative and absolute male feeding rates thus were not caused by differential access to feeding grounds.
100
~
,
75 (2) (2)
~ 5o
(2) (3X~)
(2)
ILl
< 25 ~;
(5)
Statistical Procedure Because many of the potential factors influencing paternal care are interrelated I analysed the data using both product-moment correlation and multiple linear regression. Several variables were not normally distributed and therefore had to be transformed in order to obtain approximately normal distributions. In the analyses the following
I
lO
20 NO. OF PAIR C O P U L A T I O N S
30
Figure 1. Relative number of feedingsby male swallowsin relation to number of pair copulations. Values are mean _+sD for 1-h observation periods for different pairs in the various groups. Numbers in parentheses are number of pairs. Each male was observed for 18-23 days.
Moiler." Swallow paternity and paternal care 100
100
~" 75
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Ill
~
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25
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25 (31) ( )
(I)
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I
5
I
1'0
NO. OF EPCS
Figure 2. Relative number of feedings by male swaUows in relation to number of extra-pair copulations involving the female mate. Values given are mean +_so for l-h observation periods of different pairs in the various groups. Numbers in parentheses are number of pairs. Each male was observed for 18 23 days.
I
I
I
25 50 75 EPC FRACTION (%)
100
Figure 3. Relative number of feedings by male swallows in relation to the percentage of extra-pair copulations out of the total number of copulations involving the female mate. Values are mean + SD for 1-h observation periods for different pairs in the various groups. Numbers in parentheses are number of pairs. Each male was observed for 18-23 days.
Social Dispersion and Feeding Rates Colonial male swallows and solitarily breeding males provided a similar percentage of parental care during the entire nesting cycle (colonial: 50.0 + 11.6%, N = 38; solitary: 50.8 + 8.3%, N = 14, t = 0"01, dr= 50, NS). The variation in paternal care between pairs was, however, much larger among colonial than among solitarily breeding swallows (F= 10.82, dr=37, 13, P<0.001).
Copulations and Feeding Rates M a n y factors may influence feeding rates in birds including brood size, food availability, time of season, time of day, body size of parent and contribution of the male (Davies 1986; H o w e 1979; Joste et al. 1982; Wittenberger 1982; McGillivray 1984). Analyses of the relative rather than the absolute number of male feedings should control for all of these factors except from the contribution of the male. I have thus concentrated on such analyses, but results obtained from analyses of absolute male feeding rates are very similar, as shown below. The relative number of male feedings for each pair increased with the number of pair copulations seen during observations (r = 0'60, t = 4-50, dr= 36, P<0"001; Fig. 1). The absolute number of male feedings also increased with the number of pair copulations (r=0.44, t=2-94, d r = 3 6 , P < 0 . 0 1 ) .
100
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)
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o) (')
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'
60
Figure 4. Relative number of feedings by male swallows in relation to number of chases involving the female mate. Values are mean + SD for 1-h observation periods for different pairs in the various groups. Numbers in parentheses are number of pairs. Each male was observed for 18-23 days.
Animal Behaviour, 36, 4
1000
Table 1. Relative number of male feedings during the nestling period in relation to various variables in a multiple linear regression analysis (N= 38) Independent variable
Regression coefficient 4- SE
0.05___0.02 Absolute number of pair copulations -0.13___0.06 Absolute number of extra-pair copulations by female -0.29+0.13 Relative number of extra-pair copulations by female -- 0-004 -+ 0.002 Number of chases of female -- 0.003 4- 0.002 Arrival date of male --0"21 x 10 4-+8"16 x 10-4 Egg-laying date of female Male wing length 0.00 +0.00 Male body weight -- 0-03 -+0.01 0.17 x 10-7_ 1.44 x 10 -7 Male body condition index Male mite infection - - 0"006 + 0' 120 Male song rate 0.003 4- 0.002 Mate guarding 0.06__+0.10 Operational sex ratio 0.03 + 0.03 --0-31x10 4__+0.62x10 -4 Total number of feedings
The relative n u m b e r o f male feedings decreased with the n u m b e r of extra-pair copulations involving the m a t e (r = - 0-68, t = 5"56, df= 36, P < 0"001; Fig. 2). A similar relation was f o u n d for absolute n u m b e r o f male feedings ( r = - 0 . 5 6 , t=4'06, df= 36, P < 0"001). W h e n extra-pair copulations m a d e up a large percentage o f the total n u m b e r o f copulations, male swallows tended to feed nestlings relatively a n d absolutely less frequently t h a n w h e n extra-pair c o p u l a t i o n s h a d n o t occurred (relative n u m b e r o f male feedings: r = - 0 . 3 7 , t=2'39, df= 36, P < 0-05, Fig. 3; absolute n u m b e r o f male feedings: r = - 0 . 3 4 , t=2.19, df=36, P<0-05). Male swallows c a n n o t record extra-pair copula-
P <0.01 <0.05 <0.05 < 0.01 NS NS NS < 0.05 NS NS MS NS NS NS
tions directly, because, if present, they interfere to prevent such c o p u l a t i o n s (Moiler 1985). They may, however, record the interest t h a t n e i g h b o u r i n g males are taking in their mates from the frequency o f n e i g h b o u r s chasing their females. Some o f these chases lead to extra-pair copulations (Moiler 1985). Relative a n d absolute frequency o f male feedings decreased as the frequency of female chases by n e i g h b o u r i n g males increased (relative male feedings: r = - 0 . 7 0 , t=5.88, df=36, P < 0 . 0 0 1 , Fig. 4; absolute male feedings: r = - 0 " 7 0 , t = 5 ' 8 8 , d f = 36, P < 0 " 0 0 1 ) . Since the variables are interrelated, the results were checked in a multiple linear regression. T h e
II. Total number of male feedings during the nestling period in relation to various variables in a multiple linear regression analysis ( N = 38) Table
Independent variable
Regression coefficient_+ sE
Absolute number of pair copulations 50.79 _+20.59 Absolute number of extra-pair copulations by female -- 147.07_+62.28 Relative number of extra-pair copulations by female --3-04__+ 1.28 --3.84___ 1.52 Number of chases of female 0.45 + 0.79 Arrival date of male -- 17.28+ 12'44 Male wing length 83"64 __+65"90 Male body weight -- 13 257"62--+7920"86 Male body condition index 2"76_+ 12'35 Male mite infection 3"00 + 1"95 Male song rate 2"66 -- 1"69 Mate guarding --35'61 +28'45 Operational sex ratio Total number of feedings 0-45 -+0"06
P < 0.05 <0-05 <0.05 <0-05 MS NS NS NS NS MS NS MS < 0"001
Moiler: Swallow paternity and paternal care
1O01
Table Ill. Feeding rates of pairs with an increased number of female extra-pair copulations (experimental colonial), of experimental solitary pairs and of control pairs (controls)
Feeding rate Male feeding rate per h Female feedingrate per h Total feeding rate per h Male feedings (%) N
Colonial Solitary experimentals experimentals 5.2 + 1.7 8.6+ 1.3 13.8+2.6 36.3 +__7.2 10
12-3___3.4 10.8___2.2 23.1 +5.4 53-1 ___8.5 5
Colonial controls caught and released at night
Colonial controls caught and detained during night
11.4__+1.9 12.7___2.7 24.1 __+4-3 47.8 ___3.3 10
10.7 + 2.9 12.2+6.0 22.9+8.7 48.6__.8.2 10
Values are mean + so. All differencesbetween colonial experimental and other groups are significant (Mann-Whitney U-test, P < 0.001) whereas differences between other groups are non-significant.
relative number of male feedings was significantly related to the different variables (multiple r 2---0-56, N=38, F=2"37, df=14, 23, P<0"05, Table I). Male swallows fed young at a higher rate when pair copulations were more frequent and when extrapair copulations were absolutely and relatively infrequent (Table I). Male parental care also decreased with an increasing number of chases of the female by alien males (Table I). The absolute number of male feedings during the nestling period was more closely related to the variables than was the relative number of male feedings (multiple r2=0-88, N = 3 8 , F=12-22, df= 14, 23, P<0.001, Table II). Again, the same variables were of importance; males fed young more often when having copulated more with their mates, when extra-pair copulations were few, and when the relative number of extra-pair copulations was small. Male swallows also provided relatively little parental care if the mate had been chased frequently by male neighbours during her fertile period (Table II). The male contribution of feedings was strongly positively correlated with the total number of feedings (Table II), and swallows thus seemed to adjust their parental care in relation to the contribution of the mate. The operational sex ratio during the fertile period of the female mate affected neither the male fraction of feedings nor the absolute number of male feedings (Tables I and II). Males arriving early in spring, being in better condition, spending much time singing and guarding their mates, and carrying fewer parasitic mites should be of a higher quality than other males. None of these variables, however, was significantly related to the intensity of later paternal care (Tables I and II).
'Experimental' Extra-pair Copulations and Feeding Rates Experimental colonial females experienced 0-7+0-5 (N=10) extra-pair copulations per h whereas control females experienced no extra-pair copulations ( U = 10, N~ = 10, N2= 10, P=0-002, M~ller 1987c). Experimental solitary females did not experience any extra-pair copulations. Only a minor percentage of females (18%) have been recorded as participating in extra-pair copulations, and the absence of extra-pair copulations in the control groups did not deviate from expectation (0 versus 1.8 expected, binomial test, P=0.13). Experimental removal of colonial male swallows during the fertile period of their mates significantly reduced the relative and absolute number of male feedings during the nestling period (Table III). Female mates also decreased their feeding rates among experimental colonial pairs relative to the feeding rates of control females. The reduction of the feeding rate in the females, however, was smaller than the male reduction leading to a decrease in the relative male contribution in experimental colonial pairs (Table III). The experimental colonial group differed from both control groups in the extent of parental care whereas the two control groups did not differ from each other (Table III). Experimental solitary pairs did not deviate from any of the control groups in the extent of parental care (Table III). The length of the nestling periods were similar in the four groups (experimental colonial: 21.2_+ 1.0 days, experimental solitary: 20.8_+0.8 days, control 1:20-8_+0"6 days, control 2:20-8+0.6 days, Mann-Whitney U-test, all MS). Mean nestling weight per brood on day 15 in the nestling period
Animal Behaviour, 36, 4
1002
was also similar in the four groups (experimental colonial: 20-1 + 1-9 g, experimental solitary: 22.2+1-2 g, control l: 21.3+_1.1 g, control 2: 21-0+_1.3 g, Mann-Whitney U-test, all NS). Nestling mortality rate per brood was much larger in the experimental colonial than in any of the other groups (experimental colonial: 27_+30%, experimental solitary: 0 + 0%, control 1: 0_+ 0%, control 2: 2_+6%, Mann-Whitney U-test, U=7-5, P = 0.002, U = 10, P=0-002, U = 14, P<0.02, respectively). Nestling mortality was apparently caused by starvation.
DISCUSSION Paternal Care
My results show that male swallows provided significantly more parental care if they had copulated frequently with their mates during their fertile period and if the absolute and relative number of extra-pair copulations were few. An experimental increase in the number of extra-pair copulations experienced by the female mate and, thus, probably in the uncertainty of paternity, led to a decrease in the male contribution of feedings. The experimental treatment could have influenced the results as experimental males had to be detained longer than controls in order to obtain the difference in the frequency of extra-pair copulations. A long-lasting disturbance of experimental males may cause a reduction in future paternal care, and a larger reduction in experimental male compared with experimental female provisioning of nestlings. However, all-night detention of males in a previous year did not lead to a reduction in paternal care, and so the experimental results were probably due to differences in activities in the morning rather than differences in the extent of disturbance. The lack of reduction in the amount of parental care in experimental solitary swallows also suggests that the results are not an effect of the experimental procedure. Experimental colonial and control pairs bred at the same time of the season, were caught at a similar time in their nesting cycle and laid clutches of a similar size. Experimental colonial and control males nested in the same colonies, and effects of colony size upon food abundance or sexual activity of individuals were thus similar for all individuals. The reduction in the amount of parental care led to fledging of fewer nestlings although these nestlings fledged at a similar age and had a similar body
weight as those of the control groups. Males thus apparently provided food to the brood at a lower rate when uncertain of their paternity. This interpretation rests upon the assumption that extra-pair copulations with a certain probability can lead to fertilization. This appears to be true for the swallow according to parent-offspring regressions of tarsus length (Meller 1987a). An alternative explanation for variation in the relative contribution of the sexes to parental care is that males that are of a higher quality than their mates can afford to feed nestlings relatively little. This so-called differential-allocation hypothesis (Burley 1986) postulates that mates of attractive individuals will have to pay for this quality by making a relatively high parental investment. However, it is difficult to imagine that quality differences between mates should be greater or more common among colonial than solitarily breeding swallow pairs, as would be required to explain the larger variance in paternal care in colonies than among solitary pairs. Food abundance per individual swallow decreases with colony size, and swallows breeding in colonies thus provide less food to their nestlings per time unit than solitary breeders (Moiler 1987b). The larger variance in the extent of paternal care among colonial than solitarily breeding swallows thus cannot be attributed to the effect of food abundance. A third explanation might be that males provide little parental care because they spend time seeking extra-pair copulations. However, this is unlikely because chases and extra-pair copulations are relatively infrequent, especially during the nestling period (Moiler 1985), and occupy at most a few per cent of the time budget of breeding swallows. Sexual behaviour of swallows changes with age and young inexperienced females and old experienced males especially participate in chases and extra-pair copulations (Meller 1985). The breeding experience of pair members was positively related (A. P. Moiler, unpublished data). Experienced breeders were not spatially concentrated, e.g. in the centre of colonies (A. P. Moller, unpublished data), and the correlation between extra-pair copulations and male feeding rates therefore cannot be explained by a correlation of both factors with experience. The change in female parental care seen in the present study was expected from a theoretical point of view. If the cost of cooperative behaviour (e.g. parental care) increases for one but not another
Moiler: Swallow paternity and paternal care
member of a cooperative unit, then the individual with an increased cost is predicted to decrease its contribution, too, in order to maximize its own inclusive fitness (Chase 1980). The reduction in the amount of parental care due to the non-cooperative behaviour of the male swallow was to some extent compensated by the female mate. Experimental colonial males contributed 46-49% of the feeding rate of the male control groups whereas the experimental colonial females compensated for the low male feeding rate by contributing 68-70% of the feeding rate of the female control groups. This differential sexual willingness to provide cooperative behaviour may arise from a female-biased certainty of having contributed genetically to offspring in the nest. How can male swallows estimate their certainty of paternity? Males never witness extra-pair copulation attempts without interfering (M~ller 1985). However, males may estimate the interest that other males are taking in their mates from the number of chases. Paternal care was in fact negatively related to the number of chases of their mate by male neighbours (Tables I, II and III), and many of these chases were witnessed by the mates of the chased females. This correlation was not caused by males chasing away intruding males during the nestling period and thus spending little time feeding their own nestlings; chases were almost absent during the nestling period (see also Moiler 1985). Male swallows may also have used chases as a cue to their certainty of paternity in the experimental situation because neighbouring males frequently chased experimental colonial females after the release of experimental colonial male swallows (Moiler 1987d).
Female Costs and Benefits of Extra-pair Copulations Why do females engage in extra-pair copulations if as a result they reduce their mate's contribution to parental care? My data showed that female parental care was inversely related to male parental care, and parents thus appeared to adjust their contribution to that of their mate, perhaps as a response to the intensity of the begging calls of the nestlings. Although female swallows do not actively seek extra-pair copulations, they do not try to avoid all of them. Many extra-pair copulation attempts are refused, apparently because of the quality of the male involved (A. P. Moiler, unpub-
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lished data), but others are accepted without any resistance even by the same female (Mailer 1985, unpublished data). The benefits of extra-pair copulations have to exceed or at least equal the costs for the female to participate willingly. One suggestion is that females may benefit from copulating with already mated males of superior quality (see Moller 1985). A second is that females obtain 'helpers' to feed their young by engaging in extra-pair copulations. This, however, is not the case in the swallow. A third reason may be to avoid infanticide (Crook & Shields 1985). But females never copulated with unmated males which are most likely to practise infanticide even though such males attempted extra-pair copulations (A. P. Moiler, unpublished data). Fourth, females may benefit from extra-pair copulations by improving their chances of laying fertile eggs, e.g. if their present mate proves to be infertile. This is highly unlikely since totally infertile clutches were very rare both among colonially and solitarily breeding swallows ( N = 1083 clutches. A. P. Moller, unpublished data). Another suggestion is that males whose mates indulge in extra-pair copulations anyway would not provide much parental care. This last possibility can be excluded in this case since the pairs were assigned randomly to the experimental and the control groups. The greater variance in paternal care among colonial than solitarily breeding swallows is in agreement with the interpretation that the certainty of paternity influences male parental care. In contrast to colonial birds, solitarily breeding females never experience extra-pair copulations (Moller 1985), and only colonial females had mates that provided little food for the young. In conclusion, females may benefit from extra-pair copulations because of the 'good' genes provided by extra-pair copulation partners. One might think that attributes of male quality other than copulation activity may influence the amount of paternal care. However, it was not significantly related to measures of male quality such as body condition, time of arrival in spring, song activity, mite infection, or mate guarding. This suggests that the amount of parental care given by a male is primarily determined by his certainty of paternity, as estimated by the copulation and extra-pair copulation activity of the female and to a much smaller extent, if at all, by other male attributes. If the results presented here are general for monogamous bird species, this would have con-
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siderable i m p o r t a n c e in several fields o f behavioural ecology a n d e v o l u t i o n a r y biology. Males may estimate their certainty o f paternity f r o m intrusion rates into their territories. It m a y thus be unjustified to c o m p a r e the paternal care given by individuals w i t h o u t correcting for differences in extra-pair copulation frequency a n d the concomitant differences in paternity certainty. Paternal care c a n n o t be used as a measure o f p a r e n t a l investment (e.g. Howe 1979; W i t t e n b e r g e r 1982; McGillivray 1984) w i t h o u t taking into a c c o u n t the influence o f differences in the certainty o f paternity. Increased p a r e n t a l investment with age, which has been claimed to be due to changes in the residual reproductive value (Pugesek 1981), m a y in fact be due to age-related changes in the certainty o f paternity.
ACKNOWLEDGMENTS T. R. Birkhead, A. L u n d b e r g a n d S. U l f s t r a n d all provided constructive criticism of earlier drafts o f this paper. T h e research was s u p p o r t e d by a g r a n t from the Swedish N a t u r a l Science Research C o u n cil.
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