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Divorce and asynchronous arrival in common terns, Sterna hirundo
ANIMAL BEHAVIOUR, 1999, 58, 1123–1129 Article No. anbe.1999.1235, available online at http://www.idealibrary.com on
Divorce and asynchronous arrival in common terns, Sterna hirundo JACOB GONZA u LEZ-SOLIuS, PETER H. BECKER & HELMUT WENDELN
Institut fu ¨ r Vogelforschung ‘Vogelwarte Helgoland’ (Received 4 January 1999; initial acceptance 5 February 1999; final acceptance 13 July 1999; MS. number: 6101)
We investigated which of three hypotheses (better option, incompatibility or asynchronous arrival) best explains divorce in the common tern. One partner did not return the next year in 18.5% of 150 pairs. Among the 106 pairs in which both mates returned, the divorce rate was 18.9%. We found no significant differences in: breeding performance or condition in relation to the probability of divorce; quality of previous mates and new mates, mean age in relation to pair bond status; breeding success before and after divorce nor did this differ from breeding success of reunited pairs. Hence the better option and incompatibility hypotheses were not supported. However, divorce was more likely in pairs in which mates arrived asynchronously on the breeding grounds, supporting the asynchronous arrival hypothesis. Median arrival asynchrony for divorced pairs was 7.5 days and for reunited pairs 2 days; mates arriving more than 16 days apart always split up. About 20% of divorced birds lost breeding status in the year of divorce, probably as a consequence of their late arrival. Our results suggest that terns search for a new mate as soon as they arrive on the breeding grounds and that mates remain faithful to each other to avoid the costs of searching for a new partner. Thus, synchrony in arrival facilitates pair bond maintenance rather than asynchrony promoting divorce, since divorce appears to be a side-effect of asynchrony and not an active decision.
The better-option hypothesis suggests that divorce will take place when one mate has access to a better-quality mate to improve its own reproductive success (Davies 1989; Ens et al. 1993). In this case, the incidence of divorce is predicted to be greater among low-quality individuals because of their greater scope for improvement than good-quality individuals. To test this prediction, we can use different measures of individual quality such as reproductive success (Thomas & Coulson 1988), egg size (Reid & Boersma 1990; Bolton 1991), timing of breeding (Coulson & Porter 1985; Mills 1989; Sydeman et al. 1991), body condition (Phillips & Furness 1998; Wendeln & Becker 1999) or age (e.g. Saether 1990) in one year to compare the quality of birds that divorce or reunite in the subsequent year. The better-option hypothesis also predicts that divorce will be initiated by only one individual, which should pair with a better mate than the former one. In some species, such as the common tern, some birds lose their breeding status in the year of their divorce. This hypothesis assumes that these birds are poor-quality individuals that were deserted by their mates (Ens et al. 1993). Therefore, new mates after divorce should on average be of higher quality than former mates and the reproductive success of those birds that divorced
The causes and consequences of divorce in monogamous birds have recently attracted much attention (Black 1996a). In long-lived monogamous birds, the majority of pairs breed together for several years until one partner either dies or breeds with a different partner when both members of a pair survive to the next breeding season (i.e. the pair divorces). However, the recent proliferation of different hypotheses to explain when individuals should divorce indicates that the reasons for mate fidelity are still poorly understood (Black 1996b). Three main hypotheses may explain divorce in common terns: the better-option hypothesis, the incompatibility hypothesis and asynchronous arrival between mates on the breeding grounds (see Johnston & Ryder 1987; Choudhury 1995; Ens et al. 1996 for reviews).
Correspondence and present address: J. Gonza´lez-Soli´s, Marine Life Sciences Division, British Antarctic Survey, High Cross, Madingley Road, Cambridge CB3 0ET, U.K. (email: [email protected]). P. H. Becker and H. Wendeln are at the Institut fu¨r Vogelforschung ‘Vogelwarte Helgoland’, An der Vogelwarte 21, D-26386 Wilhelmshaven, Germany. 0003–3472/99/111123+07 $30.00/0
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is expected to increase, although the latter effect may be masked by the initial costs of changing mates (Choudhury 1995; Ens et al. 1996). On the other hand, it is often assumed that divorce is initiated by the same sex, usually by females because males arrive earlier on the breeding grounds (e.g. McNamara & Forslund 1996). In this case, we should detect an increased breeding success and/or mate quality after divorce only for this sex. Finally, divorce should decrease with age, as individuals under this hypothesis are expected eventually to find a partner of acceptable quality and thereby do not divorce. The incompatibility hypothesis suggests that a bird’s mate may not necessarily be poor in quality but their combination results in reduced fitness (Coulson 1966, 1972; Rowley 1983). Under this hypothesis, pairs will be more likely to divorce after a reproductive failure, and divorce should lead to greater reproductive success with a new mate for both members of the former pair than they had together. Quality of the previous and new mates, however, should not differ on average. Furthermore, divorce should decrease with age, since birds should detect incompatibility and search for a new partner as soon as possible. The asynchronous arrival hypothesis proposes that divorce is a side-effect of the differential arrival of mates on the breeding grounds (Coulson & Thomas 1980). A further version of this hypothesis has been proposed for blue tits, Parus caeruleus, under the name of ‘musical chair hypothesis’ (Dhondt & Adriaensen 1994) since a bird returning too late will find its ‘chair’ occupied. Long-lived birds usually reunite with their previous partners in the same territory as the year before. Divorce may occur when a bird pairs with a new partner before the previous partner has returned, that is, the previous partner has been pre-empted by a new bird that arrived earlier (Ens et al. 1996). In contrast with the other hypotheses, this one has been considered nonadaptive because divorce is triggered by the absence of the mate and therefore, on average, we do not expect any difference in reproductive success between divorced and reunited individuals in preceding or subsequent breeding attempts (Dhondt & Adriaensen 1994). Moreover, no trend with age is expected, since asynchronous arrival may occur at any age. The common tern is a long-lived migratory species that is highly philopatric to the breeding grounds. In our study colony, about 89% of adults return to breed every year (Wendeln & Becker 1998) and partners reunite on the breeding grounds. There is usually one breeding attempt a year, although some birds are able to renest when the first breeding attempt fails (e.g. Gonza´ lez-Soli´s et al. 1999a). The common tern is a monogamous species with a high degree of mate and nest site fidelity (Marples & Marples 1934; Austin 1945, 1947, 1949; Burger & Gochfeld 1991; Neubauer 1997; Gonza´ lez-Soli´s et al. 1999b, in press), but the causes and mechanisms of divorce in this species as well as its consequences are poorly known. In this study we examined the potential causes and consequences of divorce in common terns with regard to the three divorce hypotheses mentioned above.
METHODS
Study Area and Data Collection We studied a common tern colony breeding on six small artificial islands in the harbour area at Wilhelmshaven (German North Sea coast). The islands are rectangular (each 10.74.6 m) and ca. 0.9 m apart. Over the course of the study, about 90–150 pairs bred in the colony from 1992 to 1996 and about 250 pairs in 1997 and 1998. We used transponders to identify individuals (see e.g. Elbin & Burger 1994). The transponder is a microchip, implanted subcutaneously and providing an individual code of 10 alphanumeric places. It does not require a battery, has an unlimited life span and is activated and read by hand-held or stationary readers at a distance of c11 cm, regardless of the angle of scan, light or environmental conditions. We used a small transponder (Trovan ID 100, 112 mm from Trovan LD, Douglas, Isle of Man, U.K.), injected subcutaneously into the breast, allowing yearly identification without retrapping and handling. The details of marking the birds at the colony site and of identifying them remotely by an automatic antenna-system are given in Becker & Wendeln (1997). We did not observe any negative effects of this marking method on behaviour or on adult survival (Wendeln & Becker 1998) or the number of chicks fledged per pair (pairs without transponders: 1997: 0.9 chicks/pair, N=117; 1998: 0.4, N=111; one or both mates with transponder: 1997: 0.9, N=79; 1998: 0.5, N=110; Mann–Whitney U test: 1997: Z= 0.07, NS; 1998: Z= 1.20, NS). For a long-term project on the population ecology of the common tern, in 1992 we started to fit all fledged chicks of this colony and some adult birds (101) with transponders. Since 1993, we have checked each nest in the colony for individuals bearing transponders by placing one antenna at the nest during the incubation period for 1–2 days. When we put the antenna in place, the terns returned to the nest and started incubation immediately and we did not observe any change in their behaviour. By 1998, 186 marked breeders had been identified. A small wall 60 cm high surrounds each of the islands. These are equipped with 42 locations for the terns to land and to rest (resting boxes). Antennas and balances are regularly distributed among the boxes for identification and automatic recording of the terns’ mass over the breeding season (for details see Wendeln & Becker 1996). Laying date, egg size, laying order and the fate of the eggs and chicks were obtained from colony checks every 2–3 days during the breeding period, limited to 1 h. The terns returned to their nest and continued incubation, brooding or chick feeding during the check or straight afterwards. We measured the maximum length and breadth of the eggs to the nearest 0.1 mm using vernier callipers. The age of many adults was known because they were ringed as chicks. Adults were sexed by their courtship and copulation behaviour. The investigations were done under licences from the Niedersaechsisches Landesverwaltungsamt, Hannover, and the Bezirksregierung Weser-Ems, Oldenburg (Tierschutzangelegenheiten; Nationalparkverwaltung).
GONZA u LEZ-SOLIuS ET AL.: DIVORCE IN COMMON TERNS
Definitions and Statistics For each nest, we recorded the laying date as the number of pentads (5-day periods) elapsed from 1 January to the laying of the first egg in a clutch. Afterwards we transformed the number of pentads to the corresponding number of days to facilitate its interpretation. We estimated egg volume as the mean volume of eggs in a clutch. Egg volume in cm3 was estimated from external measurements (in mm) using the expression: volume=egg lengthbreadth2/1000 (Harris 1964). Note that this expression is not the actual egg volume, but an estimator of it. We measured the asynchrony in arrival at the breeding grounds between partners as the absolute difference in days between their arrival for the respective year. Some birds were not identified until the nest was checked. To overcome this potential bias, we used cases only if the arrival dates of both mates were recorded at least 7 days ahead of their laying date. The relationship between skeletal size and body mass in our colony has previously been studied from trapped adults (Wendeln et al. 1997). No association was detected, suggesting that the effect of quality on body mass was greater than the effect of skeletal size. Thus, we recorded body condition as the average mass of an individual bird for both the incubation and chick-rearing periods (Wendeln & Becker 1999). Similarly, we obtained a measure of body condition at the beginning of the season from the average of the mass records for each individual on its first day at the colony site, provided that this day was at least 7 days before the laying date. Individual values of body mass, laying date and fledgling production are known to be consistent between years and to reflect individual quality in seabirds (e.g. Coulson & Porter 1985; Sydeman & Eddy 1995; Phillips & Furness 1998; Wendeln & Becker 1999). We estimated the individual quality of former and new partners, therefore, as the individual average values of these parameters over all years recorded, for those birds for which data from at least 2 years were available. To test simultaneously for the influence of the previous breeding success (0–3 chicks fledged or 0 versus at least one chick fledged) and the arrival asynchrony (0–58 days) (independent variables) on the probability of divorce (divorced versus reunited, dependent variable) we performed a stepwise logistic regression. Information on certain variables was lacking for some cases and therefore sample sizes vary somewhat between analyses. All tests are two tailed. Results are presented as XSD unless indicated otherwise.
Table 1. Age (years) of common terns (X±SD) in relation to their pair bond status
Reunited Divorced Widowed
N
Males
N
Females
48 13 6
7.66±3.16 6.92±3.63 10.17±2.86
44 13 8
7.34±2.89 7.61±4.21 8.00±3.46
was not significantly different between years (G4 =3.02, P=0.55). We did not find significant differences in mean age in relation to pair bond status (Table 1) either for males (F2,64 =2.12, P=0.13) or for females (F2,62 =0.25, P=0.85). Divorced birds tended to re-pair with birds of the same age, although the correlation was not significant owing to the small sample size (r4 =0.75, P=0.08).
Influence of Breeding Performance on Divorce Breeding success (no chick fledged versus at least one chick fledged) did not have any significant effect on subsequent divorce (G1 =0.40, N=100 pairs, P=0.52). Neither did previous clutch size (G1 =0.001, N=106, P=0.98, one- and two-egg clutches pooled versus threeegg clutches). Similarly, there was no difference in the egg volume of reunited pairs (39.02.6 cm3, N=83) and those that divorced the next year (38.72.5 cm3, N=20; t101 =0.61, P=0.55).
Influence of Body Condition on Divorce There was no difference in body mass during incubation between birds that reunited (males: 135.86.6 g, N=38; females: 136.38.5 g, N=33) and those that divorced the next year (males: 133.17.1 g, N=11; females: 140.09.1 g, N=8; males: t47 =1.20, P=0.24; females: t39 = 1.10, P=0.28). Similarly, there was no difference in body mass when chicks were 21 days old between reunited birds (males: 130.05.4 g, N=33; females: 125.16.2 g, N=33) and those that divorced the next year (males: 129.08.0 g, N=9; females: 126.46.7 g, N=11; males: t40 =0.44, P=0.66; females: t42 = 0.63, P=0.53). Nevertheless, there was a tendency for reunited males to be heavier on arrival on the breeding grounds (134.110.7 g, N=46) than those males that divorced in the same year (129.36.2 g, N=10), although it was not significant (t54 =1.91, P=0.07). Females did not show any difference in mass on arrival in relation to divorce (reunited: 135.715.0 g, N=48; divorced: 134.56.5 g, N=5; t51 =0.37, P=0.71).
RESULTS Among the 130 pairs in which both mates were individually marked, mate retention between years was 66.2%. In 18.5% of pairs one partner did not return to the colony the next year (widowed males: 7.7%, N=10 pairs; widowed females: 10.8%, N=14 pairs). Among the 106 pairs in which both mates returned to the colony the next year, the divorce rate was 18.9% (N=20 pairs). The divorce rate
Quality of Former versus New Partners We did not find any difference in individual body mass between the former partners (135.97.4 g) and the new partners after divorce (134.98.0 g; paired t test: t10 =0.42, P=0.69). Similarly, we did not find any difference in individual laying date between the former partners (144.78.1 days) and the new partners after divorce
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160
100 90
155
70 60 50 20
40 30
22
20 10 0
20
Laying date (days)
80 Divorce rate (%)
1126
150
5 13
145 140
75
75
135
20
130 0
12
11
1–2 3–7 Arrival asynchrony (days)
>7
Figure 1. Percentage of divorces in common terns in relation to the number of days between the arrival of the first and second members of a pair on the breeding grounds. Numbers above bars show sample sizes.
(142.58.2; paired t test: t13 =1.37, P=0.19), or in individual fledgling production between the former partners (1.30.4 chicks) and the new partners (1.50.5 chicks; Wilcoxon signed-ranks test: T + =13.47, N=10, P=0.15).
Male Female
Male Female
Male Female
Reunited
Divorced
Widowed
Figure 2. Laying date (days from 1 January+95% CI) in relation to the pair bond status for males and females. Numbers above bars show sample sizes.
From those birds that divorced, birds breeding with a new partner arrived on the breeding grounds significantly earlier (residual arrival date 0.813.1 days, N=28) than those birds that lost their breeding status in the season of their divorce (residual arrival date 17.422.1 days, N=6; Mann–Whitney U test: Z= 2.28, P<0.05).
Breeding Status and Arrival Asynchrony Among 20 divorced pairs, nine birds (22.5%) did not breed in the year of divorce, whereas among 24 widowed birds, only one (4.2%) did not breed. The difference in the rate of loss of breeding status between divorced and widowed birds was significant (G1 =4.5, P<0.05). The loss of breeding status did not show significant differences between sexes either for divorced (G1 =1.31, P=0.25) or for widowed birds (Fisher’s exact test: P=0.42). Asynchrony in arrival between mates was higher for divorced pairs (median 7.5 days, range 0–58, N=14) than for reunited pairs (median 2 days, range 0–58, N=68; Mann–Whitney U test: Z= 2.77, P<0.01). Similarly, a stepwise logistic regression analysis showed a significant effect of arrival asynchrony between mates on probability of divorce (21 =12.96, N=82, P=0.0003, SE= 0.1510.051). Breeding success did not improve the model significantly measured as either number of chicks fledged or no chick fledged versus at least one chick fledged. A logistic model showed a predicted probability of divorce of 0.5 at 17 days of asynchrony. Overall, this model correctly classified 89% of all cases of pairs divorcing or reuniting. However, the model correctly predicted 100% of cases of pairs reuniting but only 36% of divorces, that is 64% of divorces occurred before 17 days of asynchrony. For more than half of all the pairs, mates arrived within 2 days of each other. By contrast, 71% of the divorces occurred when the arrival asynchrony was 3 days or more (Fig. 1). Among reunited pairs, the female arrived 1 day (median) earlier than the male (Wilcoxon signed-ranks test: Z= 2.77, N=68, P=0.01).
Pair Bond Status and Breeding Performance Pair bond status, that is, reunited, divorced or widowed, did not have any significant effect on breeding success, measured as at least one chick fledged versus no chick fledged, either for males (G1 =2.41, N=90, P=0.30) or for females (G2 =0.59, N=97, P=0.74). Similarly, the number of chicks fledged with the former partner did not differ from the number fledged with the new partner (Wilcoxon signed-ranks test: T + =12.79, N=9, P=0.25). We did not find any significant effect of pair bond status on clutch size or egg volume for either males or females (clutch size: males: G2 =1.49, N=90, P=0.47; females: G2 =0.33, N=97, P=0.85; egg volume: males: F2,86 =0.06, P=0.93; females: F2,95 =0.39, P=0.68). We found significant differences in laying date for both males and females in relation to their pair bond status (Fig. 2; ANOVA on log-transformed laying date to approach normality: males: F2,88 =7.27, P<0.01; females: F2,97 =14.40, P<0.0001). Differences between groups were significant between reunited–divorced for males and between reunited–divorced and reunited–widowed for females (LSD test for pairs of groups: males: reunited– divorced: P=0.001; reunited–widowed: P=0.097; divorced–widowed: P=0.499; females: reunited–divorced: P=0.003; reunited–widowed: P=0.001; divorced– widowed: P=0.145). Divorced birds laid, on average, 7.0 days later and widowed birds 8.9 days later than reunited birds. We did not find any significant difference in laying dates between males and females for either divorced (t22 =0.61, P=0.55) or widowed birds (t15 = 1.17, P=0.26).
GONZA u LEZ-SOLIuS ET AL.: DIVORCE IN COMMON TERNS
DISCUSSION In this study, mate retention between two consecutive years was 66% (N=130 pairs), very close to the 69.4% (N=74 pairs) found in Massachusetts, U.S.A (Austin 1947) and slightly higher than the 45.3% (N=87 pairs) found in Mecklenburg-Vorpommern, Germany (Neubauer 1997) for the same species. About 19% of the pairs divorced from one year to the next, similar to the values reported for most gull species, in which divorce rates range from 10.5% in red-billed gulls, Larus novaehollandiae, to 30% in glaucous-winged gulls, Larus glaucescens (see review in Mills et al. 1996). Cuthbert (1985) reported a high divorce rate among Caspian terns, Sterna caspia, with 50% (N=12) of pairs divorcing between years, which was attributed to this species’ unpredictable habitat. If divorce was initiated by one member of the pair to improve its own reproductive success, we would expect reproductive success to increase only for the ‘choosers’ that is, those birds that decided to divorce (Ens et al. 1993). Nevertheless, since some of the ‘victims’ of divorce (22.5%), presumably low-quality birds, did not breed in the year of divorce, we can expect a higher reproductive success among divorced birds that breed than in widowed or reunited birds. However, we did not find any significant difference in breeding success of reunited, divorced or widowed birds. Similarly, we did not find any difference in individual quality-related parameters assessed over at least 2 years such as laying date, body mass or individual fledgling production between the former and the new partners from divorced or widowed birds, suggesting that former partners and new partners did not differ in quality. Moreover, we did not find any relationship between body mass, age or egg volume and subsequent divorce, suggesting that individual quality or condition did not affect the probability of divorce. These results contradict the predictions of the better-option hypothesis. If the incompatibility hypothesis were true (Coulson 1972), pairs would be more likely to divorce after a reproductive failure, both birds should improve their breeding success after divorce and young birds would show a higher divorce rate than old birds. However, previous breeding success did not affect the probability of divorce and divorced birds did not improve their breeding performance. Similarly, there was no relationship between age and divorce. Divorce was more likely in pairs in which partners arrived asynchronously on the breeding grounds (Fig. 1), as is the case for kittiwakes, Rissa tridactyla (Coulson & Thomas 1980), Adelie penguins, Pygoscelis adeliae (Davis & Speirs 1990) and king penguins, Aptenodytes patagonicus (Olsson 1998; Bried et al. 1999), supporting the asynchronous arrival hypothesis as the main cause of divorce in common terns. In our study, the majority of divorces occurred when arrival asynchrony was 3 days or more, and all the pairs with an arrival asynchrony greater than 16 days split up. However, although divorce rate increased with arrival asynchrony, we still found that 64% of divorces occurred before the 16-day threshold. Stochastic events in mate assessment and the
establishment of a new pair bond may explain the variability found in divorce rates. The arrival asynchrony hypothesis may be particularly important among those species where male and female arrive on similar dates on the colony site. In many seabird species, the male arrives earlier to set up the territory and females visit it until pair formation occurs (e.g. Mills et al. 1996; Williams 1996). By contrast, female common terns arrived on the breeding grounds on average 1 day earlier than males, which may lead to the pre-emption of late-arriving females (Ens et al. 1996). The fact that within-season divorce has never been observed in terns (Ashmole 1963; Cuthbert 1985; Massey & Fancher 1989) also supports the arrival asynchrony hypothesis. Common terns usually breed once a year. However, some birds are able to renest when the first breeding attempt has failed and occasionally some pairs nest twice (Gonza´ lez-Soli´s et al. 1999a). If the arrival asynchrony hypothesis is true, we would expect birds to remate in the same breeding season, since after the first breeding attempt both members of the pair are already in the colony site. In support of this, in our colony, none of the pairs divorced between two consecutive breeding attempts in the same year (Gonza´ lez-Soli´s et al. 1999b). Mills et al. (1996) suggested that one consequence of divorce in red-billed gulls is the loss of breeding status: overall, 60% of females and 31% of males changing mates did not breed in the year of divorce. In the common tern, about 20% of the divorced birds lost their breeding status in that season. If the loss of breeding status is a consequence of mate change, widowed birds should have nonbreeding rates similar to those of divorced birds. However, widowed birds lost their breeding status only occasionally. Indeed, among divorced birds, those that lost their breeding status arrived at the colony site significantly later than those birds that bred in the year of divorce. Late arrival on the breeding grounds can result in loss of breeding status because potential partners are scarcer; the probability of breeding successfully and the offspring reproductive value usually decrease over the season (for a review see Moreno 1998). Thus, in common terns, the loss of breeding status appears to be a consequence not of divorce but of late arrival, which in turn leads to the pre-emption of the late-arriving birds. One of the most important costs of mate fidelity is waiting for the previous partner to return to the breeding grounds (e.g. Black 1996b; Mills et al. 1996). Waiting may reduce breeding success because of the seasonal decline or might be a sign that the partner has died or is in poorer condition than the first to arrive. In this study, although mate fidelity was high (81%), we found no clear evidence that terns wait for the previous partner. First, divorced terns tended to re-pair with terns of the same age. Seabirds arrive earlier on the breeding grounds as they get older (e.g. Coulson & Horobin 1976; Coulson & Thomas 1983), which is usually interpreted as an improvement in quality since early breeding is commonly correlated with fitness (De Forest & Gaston 1996 and references therein; Moreno 1998). The tendency of divorced terns to re-pair with terns of the same age probably reflects an assortative mating related to the arrival dates, suggesting that birds
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search for a new partner as soon as they arrive at the colony site. Second, we found no significant differences in the onset of laying between divorced and widowed birds. If a bird is going to divorce it should do so as soon as possible to avoid the cost of waiting for its previous partner and to improve its chances of finding a new mate. Indeed, in ring-billed gulls, Larus delawarensis, divorce appears to occur at the end of the previous season (Fetterolf 1984). Thus, the significant delay in the onset of laying observed for divorced birds should correspond to the time needed for mate assessment (Sullivan 1994) and the establishment of a new pair bond (Mills 1973). In common terns, this period is probably about 7 days, since divorced birds showed an average delay of 7 days in the timing of breeding compared with reunited pairs (Fig. 2). In the case of widowed birds, if mate fidelity leads to birds waiting a while for their former partners (Mills et al. 1996), we should find an additional delay in the onset of laying compared with divorced birds. Thus, differences in the timing of breeding between divorced and widowed birds would correspond to the time a bird spends waiting for the former mate before searching for a new one. However, widowed birds showed a delay of only 2 days in the timing of breeding compared with divorced birds, and the difference was not significant. Similar results have been reported by Coulson (1972) for kittiwakes. Thus, widowed birds seem to search for a new mate at the same time as divorced birds, suggesting again that terns search for a new mate as soon as they arrive at the colony site. Breeding delay after mate change has also been found in gulls (4.6 days in kittiwakes: Coulson 1966; 4 days in red-billed gulls: Mills et al. 1996). The breeding season is often short for terns and gulls. As mentioned above, breeding success decreases as the season progresses and therefore we would expect to find an adverse effect of delays incurred by divorced and widowed birds on breeding success. In this study, however, we could not demonstrate any cost linked to the delays after mate change, probably because effects of 1 week of delay on breeding success were not strong enough to be detected by comparing a few pairs. Indeed, it would be difficult to distinguish the effects of mate familiarity versus late breeding, since both can negatively affect other breeding performance parameters. Late breeding, however, may also have some adverse effects on fitness beyond the natal stage, since later fledging may decrease juvenile survival as well as probability of recruitment (Spear & Nur 1994). Mate fidelity may enhance reproductive success mainly through the benefits of mate familiarity or by reducing the costs involved in mate sampling (e.g. Black 1996b; Ens et al. 1996). If mate familiarity promotes mate fidelity, the costs of mate fidelity, in terms of waiting for the previous partner, should be outweighed by mate familiarity enhancing reproductive success. However, we did not find any significant drop in reproductive performance when birds changed mates, apart from later breeding, suggesting that mate familiarity did not strongly affect reproductive success. Our results suggest that the high rate of mate fidelity in common terns is mainly the result of the birds avoiding the costs of searching for a new mate. Males and females arrived at the colony on
similar dates. In such circumstances, the best reproductive strategy may be to search for a new mate immediately after arrival while waiting for the previous partner. If the arrival asynchrony between mates is less than the time needed to find a new mate, birds should remate with the previous partner in order to breed as soon as possible. However, the more delayed is the previous partner, the more likely it is to be pre-empted. In this case, synchrony in arrival facilitates pair bond maintenance rather than asynchrony promoting divorce, since divorce is a side-effect of asynchrony and not an active decision. Acknowledgments This study was supported by the Deutsche Forschungsgemeinschaft (Be 916/3) and the Direccio´ n General de Investigacio´ n Cienti´fica del Ministerio de Educacio´ n y Ciencia Espan ˜ ol (PF960037747430). We thank M. Wagener for his help in the field and J. P. Croxall, F. Bairlein, J. Freire, K. Barlow, C. Hill and an anonymous referee for their helpful comments on the manuscript. We also thank Trovan, Cologne, Germany for financial support by providing transponders. References Ashmole, N. P. 1963. The biology of the wideawake or sooty tern Sterna fuscata on Ascension Island. Ibis, 103b, 297–364. Austin, O. L. 1945. The role of longevity in the successful breeding by the common tern (Sterna hirundo). Bird Banding, 16, 21–28. Austin, O. L. 1947. A study of the mating of the common tern (Sterna hirundo). Bird Banding, 18, 116. Austin, O. L. 1949. Site tenacity, a behaviour trait of the common tern (Sterna hirundo). Bird Banding, 20, 1–39. Becker, P. H. & Wendeln, H. 1997. A new application for transponders in population ecology of the common tern. Condor, 99, 534–538. Black, J. M. (Ed.) 1996a. Partnerships in Birds: the Study of Monogamy. Oxford: Oxford University Press. Black, J. M. 1996b. Introduction: pair bonds and partnerships. In: Partnerships in Birds: the Study of Monogamy (Ed. by J. M. Black), pp. 3–20. Oxford: Oxford University Press. Bolton, M. 1991. Determinants of chick survival in the lesser black-backed gull: relative contributions of egg size and parental quality. Journal of Animal Ecology, 60, 949–960. Bried, J., Jiguet, F. & Jouventin, P. 1999. Why do Aptenodytes penguins have high divorce rates? Auk, 116, 504–512. Burger, J. & Gochfeld, M. 1991. The Common Tern. New York: Columbia University Press. Choudhury, S. 1995. Divorce in birds: a review of the hypotheses. Animal Behaviour, 50, 413–429. Coulson, J. C. 1966. The influence of the pair-bond and age on the breeding biology of the kittiwake gull Rissa tridactyla. Journal of Animal Ecology, 35, 269–279. Coulson, J. C. 1972. The significance of the pair-bond in the kittiwake. In: Proceedings of the XVth International Ornithological Congress (Ed. by K. H. Voous), pp. 424–433. Leiden: E. J. Brill. Coulson, J. C. & Horobin, J. 1976. The influence of age on the breeding biology and survival of the Arctic tern Sterna paradisaea. Journal of Zoology, 178, 247–260. Coulson, J. C. & Porter, J. M. 1985. Reproductive success of the kittiwake Rissa tridactyla: the role of clutch size, chick growth rates and parental quality. Ibis, 127, 450–466.
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Coulson, J. C. & Thomas, C. 1980. A study of the factors influencing the duration of the pair-bond in the kittiwake gull Rissa tridactyla. In: Acta XVII Congressus Internationalis Ornithologici II (Ed. by R. No¨ hring), pp. 823–833. Berlin: Deutsche OrnithologenGesellschaft. Coulson, J. C. & Thomas, C. S. 1983. Mate choice in the kittiwake gull. In: Mate Choice (Ed. by P. P. G. Bateson), pp. 361–376. Cambridge: Cambridge University Press. Cuthbert, F. J. 1985. Mate retention in Caspian terns. Condor, 87, 74–78. Davies, N. B. 1989. Sexual conflict and the polygamy threshold. Animal Behaviour, 38, 226–234. Davis, L. S. & Speirs, E. A. H. 1990. Mate choice in penguins. In: Penguin Biology (Ed. by L. S. Davis & J. T. Darby), pp. 377–397. San Diego: Academic Press. De Forest, L. N. & Gaston, A. J. 1996. The effect of age on timing of breeding and reproductive success in the thick-billed murre. Ecology, 77, 1501–1511. Dhondt, A. A. & Adriaensen, F. 1994. Causes and effects of divorce in the blue tit Parus caeruleus. Journal of Animal Ecology, 63, 979–987. Elbin, S. B. & Burger, J. 1994. Implantable microchips for individual identification in wild and captive populations. Wildlife Society Bulletin, 22, 677–683. Ens, B. J., Safriel, U. N. & Harris, M. P. 1993. Divorce in the long-lived and monogamous oystercatchers, Haematopus ostralegus: incompatibility or choosing the better option? Animal Behaviour, 45, 1199–1217. Ens, B. J., Choudhury, S. & Black, J. M. 1996. Mate fidelity and divorce in monogamous birds. In: Partnerships in Birds: the Study of Monogamy (Ed. by J. M. Black), pp. 344–401. Oxford: Oxford University Press. Fetterolf, P. M. 1984. Pairing behavior and pair dissolution by ring-billed gulls during the post-breeding period. Wilson Bulletin, 96, 711–714. Gonza´lez-Soli´s, J., Wendeln, H. & Becker, P. H. 1999a. Nest-site turnover in common terns: possible problems with renest studies. Ibis, 141, 500–502. Gonza´lez-Soli´s, J., Wendeln, H. & Becker, P. H. 1999b. Within and between season nest-site and mate fidelity in common terns (Sterna hirundo). Journal fu¨r Ornithologie, 140, 291–298. Gonza´lez-Soli´s, J., Becker, P. H. & Wendeln, H. In press. Causes and benefits of nest-site fidelity in common tern. Biologia e Conservazione della Fauna. Harris, M. P. 1964. Aspects of the breeding biology of the gulls Larus argentatus, L. fuscus and L. marinus. Ibis, 106, 432–456. Johnston, V. H. & Ryder, J. P. 1987. Divorce in larids: a review. Colonial Waterbirds, 10, 16–26. McNamara, J. M. & Forslund, P. 1996. Divorce rates in birds: predictions from an optimization model. American Naturalist, 147, 609–640. Marples, G. & Marples, A. 1934. Sea Terns or Sea Swallows. London: Country Life. Massey, B. W. & Fancher, J. M. 1989. Renesting by California least terns. Journal of Field Ornithology, 60, 350–357.
Mills, J. A. 1973. The influence of age and pair-bond on the breeding biology of the red-billed gull Larus novaehollandiae scopulinus. Journal of Animal Ecology, 42, 147–162. Mills, J. A. 1989. Red-billed gull. In: Lifetime Reproduction in Birds (Ed. by I. Newton), pp. 387–404. London: Academic Press. Mills, J. A., Yarrall, J. W. & Mills, D. A. 1996. Causes and consequences of mate fidelity in red-billed gulls. In: Partnerships in Birds: the Study of Monogamy (Ed. by J. M. Black), pp. 286–304. Oxford: Oxford University Press. Moreno, J. 1998. The determination of seasonal decline in breeding success in seabirds. Etologi´a, 69, 17–31. Neubauer, W. 1997. Beziehungen zwischen Paarbindung, Alter und Bruterfolg bei der Flusseeschwalbe Sterna hirundo. Berichte aus der Vogelwarte Hiddensee, 14, 37–45. Olsson, O. 1998. Divorce in king penguins: asynchrony, expensive fat storing and ideal free mate choice. Oikos, 83, 574–581. Phillips, R. A. & Furness, R. W. 1998. Repeatability of breeding parameters in Arctic skuas. Journal of Avian Biology, 29, 190–196. Reid, W. V. & Boersma, P. D. 1990. Parental quality and selection on egg size in the magellanic penguin. Evolution, 44, 1780–1786. Rowley, I. 1983. Re-mating in birds. In: Mate Choice (Ed. by P. P. G. Bateson), pp. 331–360. Cambridge: Cambridge University Press. Saether, B. 1990. Age-specific variation in reproductive performance of birds. In: Current Ornithology (Ed. by D. M. Power), pp. 251–283. New York: Plenum. Spear, L. & Nur, N. 1994. Brood size, hatching order and hatching date: effects on four life-history stages from hatching to recruitment in western gulls. Journal of Animal Ecology, 63, 283–298. Sullivan, M. S. 1994. Mate choice as an information gathering process under time constraint: implication for behaviour and signal design. Animal Behaviour, 47, 141–151. Sydeman, W. J. & Eddy, J. O. 1995. Repeatability in laying date and its relationship to individual quality for common murres. Condor, 97, 1048–1052. Sydeman, W. J., Penniman, J. F., Penniman, T. M., Pyle, P. & Ainley, D. G. 1991. Breeding performance in the western gull: effects of parental age, timing of breeding and year in relation to food availability. Journal of Animal Ecology, 60, 135–149. Thomas, C. S. & Coulson, J. C. 1988. Reproductive succes of kittiwake gulls, Rissa tridactyla. In: Reproductive Success (Ed. by T. H. Clutton-Brock), pp. 251–262. Chicago: University of Chicago Press. Wendeln, H. & Becker, P. H. 1996. Body mass change in breeding common terns (Sterna hirundo). Bird Study, 43, 85–95. Wendeln, H. & Becker, P. H. 1998. Populationsbiologische Untersuchungen an einer Kolonie der Flussseeschwalbe Sterna hirundo. Vogelwelt, 119, 209–213. Wendeln, H. & Becker, P. H. 1999. Effects of parental quality and effort on the reproduction of common terns. Journal of Animal Ecology, 63, 205–214. Wendeln, H., Becker, P. H. & Wagener, M. 1997. Beziehungen zwischen Ko¨ rpermasse und Ko¨ rpergro¨ ße bei Paarpartnern der Flußeeschwalbe (Sterna hirundo). Vogelwarte, 39, 141–148. Williams, T. D. 1996. Mate fidelity in penguins. In: Partnerships in Birds: the Study of Monogamy (Ed. by J. M. Black), pp. 268–285. Oxford: Oxford University Press.
1129
Divorce and asynchronous arrival in common terns, Sterna hirundo JACOB GONZA u LEZ-SOLIuS, PETER H. BECKER & HELMUT WENDELN
Institut fu ¨ r Vogelforschung ‘Vogelwarte Helgoland’ (Received 4 January 1999; initial acceptance 5 February 1999; final acceptance 13 July 1999; MS. number: 6101)
We investigated which of three hypotheses (better option, incompatibility or asynchronous arrival) best explains divorce in the common tern. One partner did not return the next year in 18.5% of 150 pairs. Among the 106 pairs in which both mates returned, the divorce rate was 18.9%. We found no significant differences in: breeding performance or condition in relation to the probability of divorce; quality of previous mates and new mates, mean age in relation to pair bond status; breeding success before and after divorce nor did this differ from breeding success of reunited pairs. Hence the better option and incompatibility hypotheses were not supported. However, divorce was more likely in pairs in which mates arrived asynchronously on the breeding grounds, supporting the asynchronous arrival hypothesis. Median arrival asynchrony for divorced pairs was 7.5 days and for reunited pairs 2 days; mates arriving more than 16 days apart always split up. About 20% of divorced birds lost breeding status in the year of divorce, probably as a consequence of their late arrival. Our results suggest that terns search for a new mate as soon as they arrive on the breeding grounds and that mates remain faithful to each other to avoid the costs of searching for a new partner. Thus, synchrony in arrival facilitates pair bond maintenance rather than asynchrony promoting divorce, since divorce appears to be a side-effect of asynchrony and not an active decision.
The better-option hypothesis suggests that divorce will take place when one mate has access to a better-quality mate to improve its own reproductive success (Davies 1989; Ens et al. 1993). In this case, the incidence of divorce is predicted to be greater among low-quality individuals because of their greater scope for improvement than good-quality individuals. To test this prediction, we can use different measures of individual quality such as reproductive success (Thomas & Coulson 1988), egg size (Reid & Boersma 1990; Bolton 1991), timing of breeding (Coulson & Porter 1985; Mills 1989; Sydeman et al. 1991), body condition (Phillips & Furness 1998; Wendeln & Becker 1999) or age (e.g. Saether 1990) in one year to compare the quality of birds that divorce or reunite in the subsequent year. The better-option hypothesis also predicts that divorce will be initiated by only one individual, which should pair with a better mate than the former one. In some species, such as the common tern, some birds lose their breeding status in the year of their divorce. This hypothesis assumes that these birds are poor-quality individuals that were deserted by their mates (Ens et al. 1993). Therefore, new mates after divorce should on average be of higher quality than former mates and the reproductive success of those birds that divorced
The causes and consequences of divorce in monogamous birds have recently attracted much attention (Black 1996a). In long-lived monogamous birds, the majority of pairs breed together for several years until one partner either dies or breeds with a different partner when both members of a pair survive to the next breeding season (i.e. the pair divorces). However, the recent proliferation of different hypotheses to explain when individuals should divorce indicates that the reasons for mate fidelity are still poorly understood (Black 1996b). Three main hypotheses may explain divorce in common terns: the better-option hypothesis, the incompatibility hypothesis and asynchronous arrival between mates on the breeding grounds (see Johnston & Ryder 1987; Choudhury 1995; Ens et al. 1996 for reviews).
Correspondence and present address: J. Gonza´lez-Soli´s, Marine Life Sciences Division, British Antarctic Survey, High Cross, Madingley Road, Cambridge CB3 0ET, U.K. (email: [email protected]). P. H. Becker and H. Wendeln are at the Institut fu¨r Vogelforschung ‘Vogelwarte Helgoland’, An der Vogelwarte 21, D-26386 Wilhelmshaven, Germany. 0003–3472/99/111123+07 $30.00/0
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is expected to increase, although the latter effect may be masked by the initial costs of changing mates (Choudhury 1995; Ens et al. 1996). On the other hand, it is often assumed that divorce is initiated by the same sex, usually by females because males arrive earlier on the breeding grounds (e.g. McNamara & Forslund 1996). In this case, we should detect an increased breeding success and/or mate quality after divorce only for this sex. Finally, divorce should decrease with age, as individuals under this hypothesis are expected eventually to find a partner of acceptable quality and thereby do not divorce. The incompatibility hypothesis suggests that a bird’s mate may not necessarily be poor in quality but their combination results in reduced fitness (Coulson 1966, 1972; Rowley 1983). Under this hypothesis, pairs will be more likely to divorce after a reproductive failure, and divorce should lead to greater reproductive success with a new mate for both members of the former pair than they had together. Quality of the previous and new mates, however, should not differ on average. Furthermore, divorce should decrease with age, since birds should detect incompatibility and search for a new partner as soon as possible. The asynchronous arrival hypothesis proposes that divorce is a side-effect of the differential arrival of mates on the breeding grounds (Coulson & Thomas 1980). A further version of this hypothesis has been proposed for blue tits, Parus caeruleus, under the name of ‘musical chair hypothesis’ (Dhondt & Adriaensen 1994) since a bird returning too late will find its ‘chair’ occupied. Long-lived birds usually reunite with their previous partners in the same territory as the year before. Divorce may occur when a bird pairs with a new partner before the previous partner has returned, that is, the previous partner has been pre-empted by a new bird that arrived earlier (Ens et al. 1996). In contrast with the other hypotheses, this one has been considered nonadaptive because divorce is triggered by the absence of the mate and therefore, on average, we do not expect any difference in reproductive success between divorced and reunited individuals in preceding or subsequent breeding attempts (Dhondt & Adriaensen 1994). Moreover, no trend with age is expected, since asynchronous arrival may occur at any age. The common tern is a long-lived migratory species that is highly philopatric to the breeding grounds. In our study colony, about 89% of adults return to breed every year (Wendeln & Becker 1998) and partners reunite on the breeding grounds. There is usually one breeding attempt a year, although some birds are able to renest when the first breeding attempt fails (e.g. Gonza´ lez-Soli´s et al. 1999a). The common tern is a monogamous species with a high degree of mate and nest site fidelity (Marples & Marples 1934; Austin 1945, 1947, 1949; Burger & Gochfeld 1991; Neubauer 1997; Gonza´ lez-Soli´s et al. 1999b, in press), but the causes and mechanisms of divorce in this species as well as its consequences are poorly known. In this study we examined the potential causes and consequences of divorce in common terns with regard to the three divorce hypotheses mentioned above.
METHODS
Study Area and Data Collection We studied a common tern colony breeding on six small artificial islands in the harbour area at Wilhelmshaven (German North Sea coast). The islands are rectangular (each 10.74.6 m) and ca. 0.9 m apart. Over the course of the study, about 90–150 pairs bred in the colony from 1992 to 1996 and about 250 pairs in 1997 and 1998. We used transponders to identify individuals (see e.g. Elbin & Burger 1994). The transponder is a microchip, implanted subcutaneously and providing an individual code of 10 alphanumeric places. It does not require a battery, has an unlimited life span and is activated and read by hand-held or stationary readers at a distance of c11 cm, regardless of the angle of scan, light or environmental conditions. We used a small transponder (Trovan ID 100, 112 mm from Trovan LD, Douglas, Isle of Man, U.K.), injected subcutaneously into the breast, allowing yearly identification without retrapping and handling. The details of marking the birds at the colony site and of identifying them remotely by an automatic antenna-system are given in Becker & Wendeln (1997). We did not observe any negative effects of this marking method on behaviour or on adult survival (Wendeln & Becker 1998) or the number of chicks fledged per pair (pairs without transponders: 1997: 0.9 chicks/pair, N=117; 1998: 0.4, N=111; one or both mates with transponder: 1997: 0.9, N=79; 1998: 0.5, N=110; Mann–Whitney U test: 1997: Z= 0.07, NS; 1998: Z= 1.20, NS). For a long-term project on the population ecology of the common tern, in 1992 we started to fit all fledged chicks of this colony and some adult birds (101) with transponders. Since 1993, we have checked each nest in the colony for individuals bearing transponders by placing one antenna at the nest during the incubation period for 1–2 days. When we put the antenna in place, the terns returned to the nest and started incubation immediately and we did not observe any change in their behaviour. By 1998, 186 marked breeders had been identified. A small wall 60 cm high surrounds each of the islands. These are equipped with 42 locations for the terns to land and to rest (resting boxes). Antennas and balances are regularly distributed among the boxes for identification and automatic recording of the terns’ mass over the breeding season (for details see Wendeln & Becker 1996). Laying date, egg size, laying order and the fate of the eggs and chicks were obtained from colony checks every 2–3 days during the breeding period, limited to 1 h. The terns returned to their nest and continued incubation, brooding or chick feeding during the check or straight afterwards. We measured the maximum length and breadth of the eggs to the nearest 0.1 mm using vernier callipers. The age of many adults was known because they were ringed as chicks. Adults were sexed by their courtship and copulation behaviour. The investigations were done under licences from the Niedersaechsisches Landesverwaltungsamt, Hannover, and the Bezirksregierung Weser-Ems, Oldenburg (Tierschutzangelegenheiten; Nationalparkverwaltung).
GONZA u LEZ-SOLIuS ET AL.: DIVORCE IN COMMON TERNS
Definitions and Statistics For each nest, we recorded the laying date as the number of pentads (5-day periods) elapsed from 1 January to the laying of the first egg in a clutch. Afterwards we transformed the number of pentads to the corresponding number of days to facilitate its interpretation. We estimated egg volume as the mean volume of eggs in a clutch. Egg volume in cm3 was estimated from external measurements (in mm) using the expression: volume=egg lengthbreadth2/1000 (Harris 1964). Note that this expression is not the actual egg volume, but an estimator of it. We measured the asynchrony in arrival at the breeding grounds between partners as the absolute difference in days between their arrival for the respective year. Some birds were not identified until the nest was checked. To overcome this potential bias, we used cases only if the arrival dates of both mates were recorded at least 7 days ahead of their laying date. The relationship between skeletal size and body mass in our colony has previously been studied from trapped adults (Wendeln et al. 1997). No association was detected, suggesting that the effect of quality on body mass was greater than the effect of skeletal size. Thus, we recorded body condition as the average mass of an individual bird for both the incubation and chick-rearing periods (Wendeln & Becker 1999). Similarly, we obtained a measure of body condition at the beginning of the season from the average of the mass records for each individual on its first day at the colony site, provided that this day was at least 7 days before the laying date. Individual values of body mass, laying date and fledgling production are known to be consistent between years and to reflect individual quality in seabirds (e.g. Coulson & Porter 1985; Sydeman & Eddy 1995; Phillips & Furness 1998; Wendeln & Becker 1999). We estimated the individual quality of former and new partners, therefore, as the individual average values of these parameters over all years recorded, for those birds for which data from at least 2 years were available. To test simultaneously for the influence of the previous breeding success (0–3 chicks fledged or 0 versus at least one chick fledged) and the arrival asynchrony (0–58 days) (independent variables) on the probability of divorce (divorced versus reunited, dependent variable) we performed a stepwise logistic regression. Information on certain variables was lacking for some cases and therefore sample sizes vary somewhat between analyses. All tests are two tailed. Results are presented as XSD unless indicated otherwise.
Table 1. Age (years) of common terns (X±SD) in relation to their pair bond status
Reunited Divorced Widowed
N
Males
N
Females
48 13 6
7.66±3.16 6.92±3.63 10.17±2.86
44 13 8
7.34±2.89 7.61±4.21 8.00±3.46
was not significantly different between years (G4 =3.02, P=0.55). We did not find significant differences in mean age in relation to pair bond status (Table 1) either for males (F2,64 =2.12, P=0.13) or for females (F2,62 =0.25, P=0.85). Divorced birds tended to re-pair with birds of the same age, although the correlation was not significant owing to the small sample size (r4 =0.75, P=0.08).
Influence of Breeding Performance on Divorce Breeding success (no chick fledged versus at least one chick fledged) did not have any significant effect on subsequent divorce (G1 =0.40, N=100 pairs, P=0.52). Neither did previous clutch size (G1 =0.001, N=106, P=0.98, one- and two-egg clutches pooled versus threeegg clutches). Similarly, there was no difference in the egg volume of reunited pairs (39.02.6 cm3, N=83) and those that divorced the next year (38.72.5 cm3, N=20; t101 =0.61, P=0.55).
Influence of Body Condition on Divorce There was no difference in body mass during incubation between birds that reunited (males: 135.86.6 g, N=38; females: 136.38.5 g, N=33) and those that divorced the next year (males: 133.17.1 g, N=11; females: 140.09.1 g, N=8; males: t47 =1.20, P=0.24; females: t39 = 1.10, P=0.28). Similarly, there was no difference in body mass when chicks were 21 days old between reunited birds (males: 130.05.4 g, N=33; females: 125.16.2 g, N=33) and those that divorced the next year (males: 129.08.0 g, N=9; females: 126.46.7 g, N=11; males: t40 =0.44, P=0.66; females: t42 = 0.63, P=0.53). Nevertheless, there was a tendency for reunited males to be heavier on arrival on the breeding grounds (134.110.7 g, N=46) than those males that divorced in the same year (129.36.2 g, N=10), although it was not significant (t54 =1.91, P=0.07). Females did not show any difference in mass on arrival in relation to divorce (reunited: 135.715.0 g, N=48; divorced: 134.56.5 g, N=5; t51 =0.37, P=0.71).
RESULTS Among the 130 pairs in which both mates were individually marked, mate retention between years was 66.2%. In 18.5% of pairs one partner did not return to the colony the next year (widowed males: 7.7%, N=10 pairs; widowed females: 10.8%, N=14 pairs). Among the 106 pairs in which both mates returned to the colony the next year, the divorce rate was 18.9% (N=20 pairs). The divorce rate
Quality of Former versus New Partners We did not find any difference in individual body mass between the former partners (135.97.4 g) and the new partners after divorce (134.98.0 g; paired t test: t10 =0.42, P=0.69). Similarly, we did not find any difference in individual laying date between the former partners (144.78.1 days) and the new partners after divorce
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160
100 90
155
70 60 50 20
40 30
22
20 10 0
20
Laying date (days)
80 Divorce rate (%)
1126
150
5 13
145 140
75
75
135
20
130 0
12
11
1–2 3–7 Arrival asynchrony (days)
>7
Figure 1. Percentage of divorces in common terns in relation to the number of days between the arrival of the first and second members of a pair on the breeding grounds. Numbers above bars show sample sizes.
(142.58.2; paired t test: t13 =1.37, P=0.19), or in individual fledgling production between the former partners (1.30.4 chicks) and the new partners (1.50.5 chicks; Wilcoxon signed-ranks test: T + =13.47, N=10, P=0.15).
Male Female
Male Female
Male Female
Reunited
Divorced
Widowed
Figure 2. Laying date (days from 1 January+95% CI) in relation to the pair bond status for males and females. Numbers above bars show sample sizes.
From those birds that divorced, birds breeding with a new partner arrived on the breeding grounds significantly earlier (residual arrival date 0.813.1 days, N=28) than those birds that lost their breeding status in the season of their divorce (residual arrival date 17.422.1 days, N=6; Mann–Whitney U test: Z= 2.28, P<0.05).
Breeding Status and Arrival Asynchrony Among 20 divorced pairs, nine birds (22.5%) did not breed in the year of divorce, whereas among 24 widowed birds, only one (4.2%) did not breed. The difference in the rate of loss of breeding status between divorced and widowed birds was significant (G1 =4.5, P<0.05). The loss of breeding status did not show significant differences between sexes either for divorced (G1 =1.31, P=0.25) or for widowed birds (Fisher’s exact test: P=0.42). Asynchrony in arrival between mates was higher for divorced pairs (median 7.5 days, range 0–58, N=14) than for reunited pairs (median 2 days, range 0–58, N=68; Mann–Whitney U test: Z= 2.77, P<0.01). Similarly, a stepwise logistic regression analysis showed a significant effect of arrival asynchrony between mates on probability of divorce (21 =12.96, N=82, P=0.0003, SE= 0.1510.051). Breeding success did not improve the model significantly measured as either number of chicks fledged or no chick fledged versus at least one chick fledged. A logistic model showed a predicted probability of divorce of 0.5 at 17 days of asynchrony. Overall, this model correctly classified 89% of all cases of pairs divorcing or reuniting. However, the model correctly predicted 100% of cases of pairs reuniting but only 36% of divorces, that is 64% of divorces occurred before 17 days of asynchrony. For more than half of all the pairs, mates arrived within 2 days of each other. By contrast, 71% of the divorces occurred when the arrival asynchrony was 3 days or more (Fig. 1). Among reunited pairs, the female arrived 1 day (median) earlier than the male (Wilcoxon signed-ranks test: Z= 2.77, N=68, P=0.01).
Pair Bond Status and Breeding Performance Pair bond status, that is, reunited, divorced or widowed, did not have any significant effect on breeding success, measured as at least one chick fledged versus no chick fledged, either for males (G1 =2.41, N=90, P=0.30) or for females (G2 =0.59, N=97, P=0.74). Similarly, the number of chicks fledged with the former partner did not differ from the number fledged with the new partner (Wilcoxon signed-ranks test: T + =12.79, N=9, P=0.25). We did not find any significant effect of pair bond status on clutch size or egg volume for either males or females (clutch size: males: G2 =1.49, N=90, P=0.47; females: G2 =0.33, N=97, P=0.85; egg volume: males: F2,86 =0.06, P=0.93; females: F2,95 =0.39, P=0.68). We found significant differences in laying date for both males and females in relation to their pair bond status (Fig. 2; ANOVA on log-transformed laying date to approach normality: males: F2,88 =7.27, P<0.01; females: F2,97 =14.40, P<0.0001). Differences between groups were significant between reunited–divorced for males and between reunited–divorced and reunited–widowed for females (LSD test for pairs of groups: males: reunited– divorced: P=0.001; reunited–widowed: P=0.097; divorced–widowed: P=0.499; females: reunited–divorced: P=0.003; reunited–widowed: P=0.001; divorced– widowed: P=0.145). Divorced birds laid, on average, 7.0 days later and widowed birds 8.9 days later than reunited birds. We did not find any significant difference in laying dates between males and females for either divorced (t22 =0.61, P=0.55) or widowed birds (t15 = 1.17, P=0.26).
GONZA u LEZ-SOLIuS ET AL.: DIVORCE IN COMMON TERNS
DISCUSSION In this study, mate retention between two consecutive years was 66% (N=130 pairs), very close to the 69.4% (N=74 pairs) found in Massachusetts, U.S.A (Austin 1947) and slightly higher than the 45.3% (N=87 pairs) found in Mecklenburg-Vorpommern, Germany (Neubauer 1997) for the same species. About 19% of the pairs divorced from one year to the next, similar to the values reported for most gull species, in which divorce rates range from 10.5% in red-billed gulls, Larus novaehollandiae, to 30% in glaucous-winged gulls, Larus glaucescens (see review in Mills et al. 1996). Cuthbert (1985) reported a high divorce rate among Caspian terns, Sterna caspia, with 50% (N=12) of pairs divorcing between years, which was attributed to this species’ unpredictable habitat. If divorce was initiated by one member of the pair to improve its own reproductive success, we would expect reproductive success to increase only for the ‘choosers’ that is, those birds that decided to divorce (Ens et al. 1993). Nevertheless, since some of the ‘victims’ of divorce (22.5%), presumably low-quality birds, did not breed in the year of divorce, we can expect a higher reproductive success among divorced birds that breed than in widowed or reunited birds. However, we did not find any significant difference in breeding success of reunited, divorced or widowed birds. Similarly, we did not find any difference in individual quality-related parameters assessed over at least 2 years such as laying date, body mass or individual fledgling production between the former and the new partners from divorced or widowed birds, suggesting that former partners and new partners did not differ in quality. Moreover, we did not find any relationship between body mass, age or egg volume and subsequent divorce, suggesting that individual quality or condition did not affect the probability of divorce. These results contradict the predictions of the better-option hypothesis. If the incompatibility hypothesis were true (Coulson 1972), pairs would be more likely to divorce after a reproductive failure, both birds should improve their breeding success after divorce and young birds would show a higher divorce rate than old birds. However, previous breeding success did not affect the probability of divorce and divorced birds did not improve their breeding performance. Similarly, there was no relationship between age and divorce. Divorce was more likely in pairs in which partners arrived asynchronously on the breeding grounds (Fig. 1), as is the case for kittiwakes, Rissa tridactyla (Coulson & Thomas 1980), Adelie penguins, Pygoscelis adeliae (Davis & Speirs 1990) and king penguins, Aptenodytes patagonicus (Olsson 1998; Bried et al. 1999), supporting the asynchronous arrival hypothesis as the main cause of divorce in common terns. In our study, the majority of divorces occurred when arrival asynchrony was 3 days or more, and all the pairs with an arrival asynchrony greater than 16 days split up. However, although divorce rate increased with arrival asynchrony, we still found that 64% of divorces occurred before the 16-day threshold. Stochastic events in mate assessment and the
establishment of a new pair bond may explain the variability found in divorce rates. The arrival asynchrony hypothesis may be particularly important among those species where male and female arrive on similar dates on the colony site. In many seabird species, the male arrives earlier to set up the territory and females visit it until pair formation occurs (e.g. Mills et al. 1996; Williams 1996). By contrast, female common terns arrived on the breeding grounds on average 1 day earlier than males, which may lead to the pre-emption of late-arriving females (Ens et al. 1996). The fact that within-season divorce has never been observed in terns (Ashmole 1963; Cuthbert 1985; Massey & Fancher 1989) also supports the arrival asynchrony hypothesis. Common terns usually breed once a year. However, some birds are able to renest when the first breeding attempt has failed and occasionally some pairs nest twice (Gonza´ lez-Soli´s et al. 1999a). If the arrival asynchrony hypothesis is true, we would expect birds to remate in the same breeding season, since after the first breeding attempt both members of the pair are already in the colony site. In support of this, in our colony, none of the pairs divorced between two consecutive breeding attempts in the same year (Gonza´ lez-Soli´s et al. 1999b). Mills et al. (1996) suggested that one consequence of divorce in red-billed gulls is the loss of breeding status: overall, 60% of females and 31% of males changing mates did not breed in the year of divorce. In the common tern, about 20% of the divorced birds lost their breeding status in that season. If the loss of breeding status is a consequence of mate change, widowed birds should have nonbreeding rates similar to those of divorced birds. However, widowed birds lost their breeding status only occasionally. Indeed, among divorced birds, those that lost their breeding status arrived at the colony site significantly later than those birds that bred in the year of divorce. Late arrival on the breeding grounds can result in loss of breeding status because potential partners are scarcer; the probability of breeding successfully and the offspring reproductive value usually decrease over the season (for a review see Moreno 1998). Thus, in common terns, the loss of breeding status appears to be a consequence not of divorce but of late arrival, which in turn leads to the pre-emption of the late-arriving birds. One of the most important costs of mate fidelity is waiting for the previous partner to return to the breeding grounds (e.g. Black 1996b; Mills et al. 1996). Waiting may reduce breeding success because of the seasonal decline or might be a sign that the partner has died or is in poorer condition than the first to arrive. In this study, although mate fidelity was high (81%), we found no clear evidence that terns wait for the previous partner. First, divorced terns tended to re-pair with terns of the same age. Seabirds arrive earlier on the breeding grounds as they get older (e.g. Coulson & Horobin 1976; Coulson & Thomas 1983), which is usually interpreted as an improvement in quality since early breeding is commonly correlated with fitness (De Forest & Gaston 1996 and references therein; Moreno 1998). The tendency of divorced terns to re-pair with terns of the same age probably reflects an assortative mating related to the arrival dates, suggesting that birds
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search for a new partner as soon as they arrive at the colony site. Second, we found no significant differences in the onset of laying between divorced and widowed birds. If a bird is going to divorce it should do so as soon as possible to avoid the cost of waiting for its previous partner and to improve its chances of finding a new mate. Indeed, in ring-billed gulls, Larus delawarensis, divorce appears to occur at the end of the previous season (Fetterolf 1984). Thus, the significant delay in the onset of laying observed for divorced birds should correspond to the time needed for mate assessment (Sullivan 1994) and the establishment of a new pair bond (Mills 1973). In common terns, this period is probably about 7 days, since divorced birds showed an average delay of 7 days in the timing of breeding compared with reunited pairs (Fig. 2). In the case of widowed birds, if mate fidelity leads to birds waiting a while for their former partners (Mills et al. 1996), we should find an additional delay in the onset of laying compared with divorced birds. Thus, differences in the timing of breeding between divorced and widowed birds would correspond to the time a bird spends waiting for the former mate before searching for a new one. However, widowed birds showed a delay of only 2 days in the timing of breeding compared with divorced birds, and the difference was not significant. Similar results have been reported by Coulson (1972) for kittiwakes. Thus, widowed birds seem to search for a new mate at the same time as divorced birds, suggesting again that terns search for a new mate as soon as they arrive at the colony site. Breeding delay after mate change has also been found in gulls (4.6 days in kittiwakes: Coulson 1966; 4 days in red-billed gulls: Mills et al. 1996). The breeding season is often short for terns and gulls. As mentioned above, breeding success decreases as the season progresses and therefore we would expect to find an adverse effect of delays incurred by divorced and widowed birds on breeding success. In this study, however, we could not demonstrate any cost linked to the delays after mate change, probably because effects of 1 week of delay on breeding success were not strong enough to be detected by comparing a few pairs. Indeed, it would be difficult to distinguish the effects of mate familiarity versus late breeding, since both can negatively affect other breeding performance parameters. Late breeding, however, may also have some adverse effects on fitness beyond the natal stage, since later fledging may decrease juvenile survival as well as probability of recruitment (Spear & Nur 1994). Mate fidelity may enhance reproductive success mainly through the benefits of mate familiarity or by reducing the costs involved in mate sampling (e.g. Black 1996b; Ens et al. 1996). If mate familiarity promotes mate fidelity, the costs of mate fidelity, in terms of waiting for the previous partner, should be outweighed by mate familiarity enhancing reproductive success. However, we did not find any significant drop in reproductive performance when birds changed mates, apart from later breeding, suggesting that mate familiarity did not strongly affect reproductive success. Our results suggest that the high rate of mate fidelity in common terns is mainly the result of the birds avoiding the costs of searching for a new mate. Males and females arrived at the colony on
similar dates. In such circumstances, the best reproductive strategy may be to search for a new mate immediately after arrival while waiting for the previous partner. If the arrival asynchrony between mates is less than the time needed to find a new mate, birds should remate with the previous partner in order to breed as soon as possible. However, the more delayed is the previous partner, the more likely it is to be pre-empted. In this case, synchrony in arrival facilitates pair bond maintenance rather than asynchrony promoting divorce, since divorce is a side-effect of asynchrony and not an active decision. Acknowledgments This study was supported by the Deutsche Forschungsgemeinschaft (Be 916/3) and the Direccio´ n General de Investigacio´ n Cienti´fica del Ministerio de Educacio´ n y Ciencia Espan ˜ ol (PF960037747430). We thank M. Wagener for his help in the field and J. P. Croxall, F. Bairlein, J. Freire, K. Barlow, C. Hill and an anonymous referee for their helpful comments on the manuscript. We also thank Trovan, Cologne, Germany for financial support by providing transponders. References Ashmole, N. P. 1963. The biology of the wideawake or sooty tern Sterna fuscata on Ascension Island. Ibis, 103b, 297–364. Austin, O. L. 1945. The role of longevity in the successful breeding by the common tern (Sterna hirundo). Bird Banding, 16, 21–28. Austin, O. L. 1947. A study of the mating of the common tern (Sterna hirundo). Bird Banding, 18, 116. Austin, O. L. 1949. Site tenacity, a behaviour trait of the common tern (Sterna hirundo). Bird Banding, 20, 1–39. Becker, P. H. & Wendeln, H. 1997. A new application for transponders in population ecology of the common tern. Condor, 99, 534–538. Black, J. M. (Ed.) 1996a. Partnerships in Birds: the Study of Monogamy. Oxford: Oxford University Press. Black, J. M. 1996b. Introduction: pair bonds and partnerships. In: Partnerships in Birds: the Study of Monogamy (Ed. by J. M. Black), pp. 3–20. Oxford: Oxford University Press. Bolton, M. 1991. Determinants of chick survival in the lesser black-backed gull: relative contributions of egg size and parental quality. Journal of Animal Ecology, 60, 949–960. Bried, J., Jiguet, F. & Jouventin, P. 1999. Why do Aptenodytes penguins have high divorce rates? Auk, 116, 504–512. Burger, J. & Gochfeld, M. 1991. The Common Tern. New York: Columbia University Press. Choudhury, S. 1995. Divorce in birds: a review of the hypotheses. Animal Behaviour, 50, 413–429. Coulson, J. C. 1966. The influence of the pair-bond and age on the breeding biology of the kittiwake gull Rissa tridactyla. Journal of Animal Ecology, 35, 269–279. Coulson, J. C. 1972. The significance of the pair-bond in the kittiwake. In: Proceedings of the XVth International Ornithological Congress (Ed. by K. H. Voous), pp. 424–433. Leiden: E. J. Brill. Coulson, J. C. & Horobin, J. 1976. The influence of age on the breeding biology and survival of the Arctic tern Sterna paradisaea. Journal of Zoology, 178, 247–260. Coulson, J. C. & Porter, J. M. 1985. Reproductive success of the kittiwake Rissa tridactyla: the role of clutch size, chick growth rates and parental quality. Ibis, 127, 450–466.
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