Forms and Variation of Helping in the European Bee-Eater (Merops Apiaster)

Biologia, Bratislava, 55/5: 563—570, 2000

Forms and variation of helping in the European bee-eater (Merops apiaster)

Radovan Václav

Institute of Zoology, Slovak Academy of Sciences, Dúbravská cesta 9,SK-84209 Bratislava, Slovakia;

áclav V , R., Forms and variation of helping in the European bee-eater (Merops apiaster). Biologia, Bratislava, 55: 563—570, 2000; ISSN 0006–3088. Two breeding pairs of European bee-eaters (Merops apiaster), each accompanied by a single male helper, were observed during the breeding seasons of 1996 and 1997, respectively. Two new forms of helping behaviour were found in this species: incubation and brooding. Both helpers participated in incubation, but the patterns of this form of help, characterised by low daily activity and little effect on the time budgets of the parents, suggest that incubation by helpers may be of limited value. However, both helpers shared about a quarter of the total time spent on brooding chicks. Moreover, a division of labour between helpers and breeders seemed to occur during this period. The most marked difference in effort by helpers appeared during chick feeding. While one of the helpers completely replaced the role of an absent pair female, the second helper deserted the breeding pair shortly after chick feeding had begun and instead helped at an adjacent nest. The patterns of helping behaviour, as well as some possible suggestions for pair switching in helpers, are discussed. Key words: Merops apiaster, bee-eater, helping behaviour, cooperative breeding.

Introduction of the breeders, or incompetence of helpers to rear young (Zahavi, 1974; Emlen, 1978, 1982; Helping at the nest has been noted in many Brown, 1987). bird species (reviewed by Brown, 1987). Most Helping behaviour, and particularly the de- studies suggest that donors may gain both di- gree of relatedness between parents and helpers, rect and indirect benefits from helping. The for- has been extensively studied in bee-eaters (File- mer includes, for instance, future mate or terri- wood et al., 1978; Dyer & Fry, 1980; Emlen & tory acquisition, whereas the latter represents im- Demong, 1980; Emlen, 1981; Lessells, 1990; provement in the inclusive fitness (Brown, 1987; Jones et al., 1991; Lessells et al., 1994). There Emlen, 1991). In the vast majority of cases, help- is, however, still a lack of basic information de- ing is considered to be beneficial for the recipi- scribing helping within a species (e.g. start of help- ents, as well as for the donors of aid (Stacey ing, and forms and intensity of help). &Koenig,1990). Some authors suggest, how- In this study (presenting two study cases), ever, that helping might incur substantial cost for forms of help in the European bee-eater, Merops both helpers (Heinsohn & Cockburn, 1994) and apiaster Linnaeus, 1758 are described and show breeding birds, for instance, by increased compe- that helping behaviour in this species may be more tition for resources, interference in the courtship variable than previously thought.

563 Material and methods initiated by the attempts of the extra male to approach the female, and lasted from a few sec- The study was carried out in the southern part of Cen- tral Slovakia, near the village of Selešťany (19◦340 E, onds to long chases, lasting exceptionally more 48◦110 N). The data consist of observations of two pairs than half an hour. Usually, only males took part in of the European bee-eater with their helpers, studied these aggressive interactions. The pair female par- in the breeding seasons of 1996 and 1997, respectively. ticipated in chasing the extra male only on the day Frequency and duration of all relevant behaviour of before the extra male disappeared. After the joint the focus couples were recorded from their morning attacks against the extra male, the pair proceeded appearance at the colony until their departure in the with courtship behaviour. The extra male aban- afternoon. Observations began from the arrival of the doned the pair six days after their appearance at pairs to the nest site (10 May, 1996 and 23 May, 1997, respectively) and ended with ﬂedging of the last young the nest site, before the beginning of the female’s in the broods (26 July and 7 August, respectively). fertile period (Fig. 1a). Subsequently, a peak of The duration of nest building, the laying phase, incu- agonistic behaviour between the pair and other in- bation and chick feeding corresponded to 12, 9, 24 and dividuals in the colony occurred (Fig. 1a), but the 30 days, respectively in 1996, and 9, 10, 22 and 33 days, duration was usually only a few seconds. The ex- respectively in 1997. The birds were usually observed tra male appeared at the colony and started to every second day (in total 31 and 41 observation days build nest with a newly mated female in the time in 1996 and 1997, respectively). Since it was not possible to observe laying and when the focus pair already incubated (Fig. 1a). incubation directly, the laying phase is deﬁned as the However, soon after completion of the nest, the period after nest construction when males rapidly re- pair with extra male broke up. Later, shortly af- duced the time they spent inside nests. During this ter initial aggressive behaviour by the couple, the period, for most of the day, only females stayed in the extra male began to provide help in the form of nests, whilst males provided them with food. After ap- incubation, chick brooding and feeding (Fig. 1a).

proximately 8–14 days from the beginning of egg laying In the second case, there was no detectable ve-

when the clutch is usually complete (Lessells & A association between the focus pair and any bird y r , 1989), males started to share incubation and nest attendance by mates was very similar. It was assumed until the end of the incubation period (Fig. 1b). In that birds were incubating during this period only in comparison to the first case, this pair male was less cases when nest visits lasted longer than 5 minutes. aggressive towards other members of the colony The hatching day and hence the end of incubation and (Figs 1a, b), probably due to his subordinate (ju- the start of brooding corresponds in this paper to the venile) status. Frequent agonistic interactions oc- day when birds first brought items of food to the nest. curred only initially after the couple appeared at The end of brooding means that none of the parents or the colony (Fig. 1b), due to aggression from al- helpers stayed in the nest longer than 5 min per hour. ready settled couples. Plumage coloration was used to determine the Although this case of helping lasted only five sex and age of the birds (Lessells & Krebs, 1989). Using this method, in the first case the pair male was days, the helper participated in incubation, brood- more than two years old, whereas the pair female, as ing and chick feeding (Fig. 1b). well as the helper, was juvenile. In the second case, the pair female was at least two years old, whereas the pair Intensity and forms of help by helpers male and the helper were juveniles. Both helpers were In both cases, helpers started to provide aid dur- males. ing incubation (Figs 1a, b). Although the helpers The focus pairs with their helpers were recog- differed in the number of days during which they nised on the basis of individual differences in plumage coloration, position of missing primaries and/or sec- incubated (10 versus 2 days), the hourly average of ondaries, development of the tip feathers on the tail incubation (Fig. 2a) was low in both helpers com- and different patterns in behaviour of pair males and pared to pair males. In contrast to the total time helpers towards pair females. budgets of parents (Fig. 2a), neither of the helpers contributed considerably to incubation. Moreover, Results because helpers often did not stay in the nests alone (Figs 3a, b), assisted incubation does not Behaviour of individuals prior to the start of help- necessarily mean that parents had more time for ing other activities, for example foraging. In the first case, the extra male accompanied the Both helpers contributed about a quarter (23 observed pair from the very beginning. Four days and 24%, respectively) of the total brooding time after the first appearance of the trio at the nest (Fig. 2b), with a tendency to stay alone in the site intense air battles between the pair male and nests for longer intervals as the chicks were older the extra male were observed. Fights were mostly (Figs 3a, b). This was mainly due to the parents

564 Fig. 1. The time extra European bee-eater males spent near the observed pairs with and without providing help. The frequency of agonistic behaviour by pair males in relation to other individuals in the colony.

which were feeding the chicks, while helpers put ent, which inexplicably disappeared 11 days after their effort only to brooding – a division of labour hatching of the first chick. However feeding rates between helpers and parents. during the time when the focus pairs were accom- The difference in the amount of help provided panied by helpers shows the relative amount of by the two helpers was most obvious during chick provisioning by helpers was similar in both cases feeding (Fig. 2c). While the second helper aban- (Fig. 2c). doned the helped pair soon after chick feeding be- The second helper, which abandoned the gan, the first helper fully replaced the female par- helped pair at the beginning of chick feeding,

565 Fig. 2. The activity of European bee-eater parents when they were either assisted or non-assisted by helpers. Since the pair female disappeared from the nest in 1996, the left part of (c) shows activity of the helper before and after the female disappeared. The numbers below bars correspond to observation hours/days. The pie charts show contribution of parents and helpers during a given period.

566 Fig. 3. The time European bee-eater helpers spent in nests alone, or with at least one of the pair member during incubation and brooding. Each bar represents one day of observation.

moved to the adjacent nest of another pair, and of helpers and breeding pairs, one case of help- participated there in chick feeding. However, af- ing ended soon after the start of chick feeding, ter a week, this individual was abandoned in the whereas the second helper continued to feed chicks colony. until they fledged. Thus, a similar magnitude in the workload of parents and a helper during a Discussion short period does not allow us to predict the extent of help in the future. Hence, to extrapolate In this study, I have shown that helpers in the the overall workload of a helper from a few ob- European bee-eater may contribute to incubation, servations only and focusing on a single activ- chick brooding and provisioning of chicks. Surpris- ity (e.g. feeding rate), what is usually predicted ingly, no forms of helping behaviour other than when we try to estimate parental care, is incor- chick feeding have previously been reported in wild rect. Since it is still uncertain how helpers regulate populations of this species. These observations their helping effort (Wright, 1998; Heinsohn support similar results found by Koenig (1959) & Legge, 1999), such predictions can be rele- who detected incubation by helpers in birds breed- vant only after considering additional factors, such ing in captivity. Nevertheless, due to the low con- as territory quality, number of helpers, quality of tribution to incubation by helpers, and the weak helpers, their relatedness with helped individuals response of breeders to this form of help (see Figs or the species-specific characteristics (Komdeur, 2a, 3), the benefits of assisted incubation are ques- 1994; Cullen et al., 1996; Dickinson et al., tionable. 1996; Hatchwell & Russell, 1996; Arnold & The present study also shows that parental Owens, 1998; Hatchwell, 1999). Because these effort in helpers can vary considerably. In addition, data are absent in this work, too, the causes of the intensity of helping at one stage of breeding, variation in helping effort cannot be identified. for instance during incubation, does not predict However, one pattern of helping behaviour magnitude of helping at other stages. In this study, that has been overlooked in European bee-eaters, similar investment of both helpers during incuba- but might play an important role is the provision tion did not lead to similar activity of helpers dur- of aid sequentially to different pairs. In addition to ing chick feeding. However, it is hard to predict the case of the helper pair switch detected in one how much would helper help if the pair female in of the focus pairs, there were fluctuations in the one of the cases would not disappear. number of caretakers at several other nests in the Moreover, even within a given period, invest- colony during both breeding seasons. These obser- ment of a helper seems difficult to predict. De- vations might indicate that this form of behaviour spite the similar pattern in relative feeding rate may not be exceptional among non-breeding Eu-

567 ropean bee-eaters. Depending on the relatedness The remarkable variation in the provisioning rates between helpers and recipients of help, the pur- among European bee-eater helpers (this work, pose of the “floating” behaviour may have differ- Jones et al., 1991) may to some extent reflect vari- ent causes. ation in relatedness between helpers and helped It is known that helping kin, via an increasing pairs (Reyer, 1980; Komdeur, 1994). Shorter number of fledglings and/or their quality, may give associations between helpers and breeders as well helpers indirect benefits (Parry, 1973; Hatch- as the switching between pairs is also typical for well & Russell, 1996). In addition, helpers may helpers when assisting to non-kin (Reyer, 1990). also gain inclusive fitness by lightening the work- Therefore, it is possible that helpers in the Eu- load of parents, who are consequently able to pro- ropean bee-eater are sometimes unrelated to the duce, for instance, more clutches (Rowley, 1965; breeding pair. In this case, “floating” of helpers be- Langen & Vehrencamp, 1999). However, help- tween nests could have different explanations. The ing is costly and may increase the risk of mortality direct benefits, such as sharing paternity (Davies, (e.g. Heinsohn & Cockburn, 1994). Therefore, 1992) or future mate acquisition (Reyer, 1984) to a non-breeding individual that follows a strat- are hypothesised to be a driving force when help- egy of helping, it should pay to be choosy when ing non-kin. Helping at several nests may then rep- selecting potential pairs to help. There are at least resent a strategy of choosing a potential mate for three situations when choosing may occur. later reproduction, whereby investment of helpers First, helpers may choose a pair where both might serve as a form of display to a potential mate breeders are the helper’s relatives. In this situa- (Zahavi, 1974, 1995). In this study, when helping, tion, choosiness is expected to be lowest because parental effort did not differ considerably between genetic conflict among relatives should be also helpers. However, in the second case the helper lowest. Nevertheless, considering the helper’s fit- provided his aid at a time when food requirements ness, it might still pay helpers to seek among rel- were still low. Therefore, it would be interesting to atives those who may due to their higher compe- know whether the amount of aid provided by the tence (e.g. in parenting, or nest protection) have helpers reflected their willingness to help, as pre- a reduced risk of breeding failure. That is to say, dicted when helping kin (Brown, 1987; Emlen, helpers should try to find pairs that are less in 1991), or whether it was a prerequisite of breeders need of help. for accepting helpers (Gaston, 1978). Similarly, it Second, pair switching should be more impor- is unclear whether the helper abandoned the pair tant in situations when genetic conflict increases himself or due to rejection by the breeders. The and multiple choice should thus help to improve latter option is unlikely, however, due to the ab- the helper’s fitness. This may be the case when sence of aggressive interactions between the trio. one of the breeders is a non-relative. Here, helpers To conclude, forms and variation of helping have an opportunity to assist in rearing relatives’ behaviour suggest that the nature of helping at offspring and thus benefit indirectly. However, if the nest in the European bee-eater is more com- the unrelated breeder is the opposite sex (e.g. a plex than previously suggested. The presence of step-parent), helpers may additionally take ad- helpers at multiple nests during a season also sug- vantage of sharing paternity with their same-sex gests that the identity of helpers does not have relatives. To avoid severe conflict between rela- to always correspond with the nest at which they tives, it might be better for the helper to seek were once detected. The variation in investment a pair where the asymmetry in dominance be- strategies that can occur when helpers attend mul- tween relatives is larger, and thus avoiding major tiple nests seems to be a fertile ground for future fights (Trivers, 1974; Emlen, 1997). Conversely, research. Further studies are also necessary to re- the asymmetry between them should not prevent veal the importance of the conflict between helpers helpers sharing reproduction with their same-sex and breeders for their reproductive success. relatives (Emlen, 1997). Sexually related aggression between males in the first case in this article Acknowledgements resembles the situation in which the helper and the pair male, but not the pair female were related. I would like to thank Herbert Hoi for his patience Unfortunately, it is not known if the helper’s com- in commenting several drafts of this manuscript, Don-

ald Blomqvist for his comments and correcting lan- pensation for the absent pair female reﬂected his

guage, Kate Lessells for methodological comments, success in fathering some of the helped oﬀspring. two anonymous referees for their valuable comments The third option is that helpers may also and many other who participated in discussions on var- beneﬁt from choosing among non-relative pairs. ious topics of this paper.

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