KAZUHIRO EGUCHI*, SATOSHI YAMAGISHI, SHIGEKI ASAI, HISASHI NAGATA and TERUAKI HINO

Ecology 2002 71, Helping does not enhance reproductive success of Blackwell Science Ltd cooperatively breeding rufous vanga in Madagascar KAZUHIRO EGUCHI*, SATOSHI YAMAGISHI, SHIGEKI ASAI, HISASHI NAGATA and TERUAKI HINO *Department of Biology, Kyushu University, Fukuoka 812 8581, Japan; Department of Zoology, Kyoto University, Kyoto 606 8502, Japan; Laboratory of Wildlife Conservation, National Institute for Environmental Studies, Tsukuba 305 0053, Japan; and Kansai Research Centre, Forestry and Forest Products Research Institute, Kyoto 612 0855, Japan Summary 1. In many studies on cooperative breeding, helping by auxiliary individuals is considered to enhance the reproductive success of breeders. However, confounding factors other than helping could cause the differences. 2. The endemic Madagascan rufous vanga Schetba rufa (Vangidae) is known as a cooperatively breeding species. In order to evaluate the effect of helping in this species, we compared the reproductive success of breeding pairs helped by auxiliary birds, and pairs breeding alone, based on a 6-year study of an individually colour-banded population in the Ampijoroa Forest Station, western Madagascar. 3. This species is single-brooded. Brood reduction was rare and most cases of nesting failure were due to total loss of clutches and broods, probably as a result of predation. 4. Monogamous pairs with one to four auxiliary birds comprised 24 43% of all breeding groups. Most auxiliary birds were male offspring remaining in their natal territory. Auxiliary males provided a considerable contribution towards antipredator defence, territory defence and to the provisioning of nestlings. In about one-third of the groups, however, the auxiliary males did not help at all. Male offspring may remain in their natal territory in order to avoid harassment by other territorial individuals, and to increase the probability of territory acquisition and of copulation with unrelated breeding females. 5. The probability of breeding successfully was higher, and the number of fledglings produced was larger among pairs with auxiliary birds than among those breeding alone. However, provisioning by auxiliaries neither enhanced the growth rate of nestlings, nor reduced the number of days they required to fledge. 6. A pair-match comparison of the same pairs between years with and without auxiliaries showed no effect of group size on their reproductive success. Even provisioning by auxiliaries did not affect the reproductive success. 7. Pairs accompanied by auxiliary birds for more than 1 year enjoyed higher reproductive success even in those years when they were without auxiliaries than did pairs always breeding alone. 8. Neither the simple presence of auxiliaries nor their helping behaviour enhanced the reproductive success of breeding pairs. The quality of the breeding pair and/or their territory may have affected their reproductive success and, as a result, increased the number of auxiliaries. Key-words: cooperative breeding, delayed dispersal, helpers-at-the-nest, Madagascar, Schetba rufa. Ecology (2002) 71, Introduction Ecological Society Correspondence: Kazuhiro Eguchi, Department of Biology, Kyushu University, Fukuoka 812 8581, Japan. Fax: + 81 92 642 2645. E-mail: kegucscb@mbox.nc.kyushuu.ac.jp Cooperative breeding has been shown to occur in more than 220 species (about 3%) of extant birds (Brown 1987). In most cases, one or more of the auxiliary birds accompanying a breeding pair assists in various tasks

124 K. Eguchi et al. such as territorial defence, antipredator defence, nestbuilding, incubation and provisioning of chicks. In many such species the presence of helping auxiliary individuals ( helpers ) has been reported as enhancing reproductive success compared with pairs without helpers (Brown 1987; Stacey & Koenig 1990; Emlen 1991). Many of the studies revealing correlations between group size and reproductive success, however, have been unable to control for confounding factors other than the helping effect (Emlen 1991; Cockburn 1998). The existence of auxiliary birds may not always be a cause, but a result of high reproductive success, brought about by the high quality of territories and/or by experienced breeders. Experimental removal of helpers from breeding groups, comparisons between groups of the same size but with different levels of helping and statistical control for confounding factors are all methods appropriate for resolving this question (Emlen & Wregge 1991; Magrath & Yezerinac 1997; Legge 2000). Some experimental studies have been unable to find any effect of helping on the reproductive success of breeders or, if there were any enhancements, the effects remained moderate (Leonard, Horn & Eden 1989; Magrath & Yezerinac 1997; Legge 2000). The significance of helping behaviour is likely to vary from species to species (Ligon 1999). It is very important to consider the adaptive significance of helping behaviour when attempting to establish whether, or not, helping per se enhances reproductive success. Therefore, in a study aiming to clarify the effects of helping, it is important to understand the processes and mechanisms operating on the population, such as nest predation, growth and survival rates of chicks and survival rates of breeders (Innes & Johnston 1996; Magrath & Yezerinac 1997). The family Vangidae is endemic to Madagascar and Comoro, and has radiated into 14 species, one of which is the Madagascan endemic rufous vanga Schetba rufa (Linnaeus) (Langrand 1990; Yamagishi & Eguchi 1996). Among the Vangidae, only two species, the rufous and Chabert s Leptopterus chabert (Müller) vangas, are known to breed cooperatively (Appert 1970), but no detailed information on their behaviour has been available previously. Recently, Yamagishi, Urano & Eguchi (1995) provided the first information about the breeding ecology of this species in the western region of Madagascar, and reported that auxiliary males, yearlings or older, assisted single breeding pairs and fed chicks. However, because both the observation time and the numbers of individuals were limited, further information on the relatedness between breeders and auxiliary birds, and the effects of helping, were not collected. Based on a 6-year study of banded individuals, we now reveal the composition of breeding groups, relatedness between breeders and auxiliary birds and the effects of helping on the reproductive success of breeding pairs. In this paper, we show that helping by auxiliary birds did not affect the reproductive success of breeders, despite the considerable involvement of auxiliary birds in antipredator defence, territorial defence and in the provisioning of chicks. STUDY AREA AND METHODS The study area was situated in a dry deciduous forest at the Ampijoroa Forest Station (16 15 S, 46 48 E), Ankarafantsika Strict Nature Reserve, about 110 km south-east of Mahajanga, western Madagascar. In 1994, the main study area was established in and around a 550 450-m quadrat (Jardin A) situated in deciduous broadleaved forest on a plateau of Cretaceous sandstone about 200 m asl. The forest is dominated by three species of Strichnos with an average canopy height of about 10 m (Razafy 1987). Within the study area, there were many trails; these were 2 m wide inside the quadrat and 3 5 m wide around the perimeter. In 1995 we cut new trails (2 5 m wide) in an area surrounding the quadrat and enlarged the study area to 1 km 1 km including the surrounding forest. The study area is within a large forest with continuous canopy. Because of the scarcity of lianas, the thin understorey and the existence of many trails, the ground is clearly visible. The climate is tropical, with a 6-month dry season from May to October and a 6-month wet season from November to April. The mean annual temperature is 26 88 C and 97% of annual precipitation falls during the wet season (Razafy 1987). The 6-year study was conducted from 1994 to 1999, from October to December in 1994, and from August or September to January in each of the other years. In advance of observation, birds were caught in mist nets. Each individual was measured, and given a unique combination of colour plastic and numbered aluminium rings. In addition 0 05 ml blood samples were collected for a further study. Because adult rufous vanga have sexually dimorphic plumage (Langrand 1990), and because even female-like plumaged 1-year-old males have distinct black spots on a white throat (Yamagishi et al. 1995), these were easily discriminated in the field. One-year-old females have buff tips on the greater wing coverts, which enabled us to discriminate 1-year-old females from older females in the hand. Almost all individuals (75 94% of the population) were banded each year. Nest-building begins in late September, and egglaying begins in early October and, if nest failure occurs, a replacement nest is built within a week of failure (Eguchi et al. 2001). Rufous vangas breed monogamously or in single breeding pairs with helpers (Yamagishi et al. 1995). By following these individuals or groups nests were easily found, and their location was then plotted on a map. Their nests are bowl-shaped, and usually located in the first fork of a tree about 4 m from the ground. Many nests were also discovered during censusing or focal individual tracking. The rufous vanga is single-brooded; breeding is confined to the 3 months from October to December, and mean clutch

125 Cooperative breeding in rufous vanga size and mean brood size are 3 7 and 3 0, respectively (Eguchi et al. 2001). Once nest-building had begun, each nest was checked at intervals of 5 7 days using a small mirror attached to a pole. During the egg-laying period and around the expected date of hatching, nests were checked every day in order to confirm clutch and brood sizes. Once egg-laying had begun, a plastic sheet daubed with grease was wrapped at breast height around the trunk of the nest tree in order to impede terrestrial predators. From the traces remaining on the sheets and from casual sightings of potential predators such as snakes near nests, however, it seems that the sheet provided little or no additional protection. Around 12 days after hatching the nestlings were caught, measured and ringed, and blood samples taken. Wing length was measured to the nearest 1 mm, using a metal ruler; bill and tarsus lengths were measured to the nearest 0 1 mm, using slide callipers and they were weighed to the nearest 0 1 g, using a digital balance. Body weights increased up to the tenth day after hatching, but then levelled off so body weight data for the period between days 10 and 16 were for use in the following analysis. Fledglings were searched for on and around the expected date of fledging. Observations were made at nests for 4 h each day from 06.00 to 10.00 h, during which time individuals visiting nests were identified, time spent at the nest was recorded and nest materials and food items being delivered were checked. The behaviour of the unaided pairs was recorded for 3 h each day from 06.00 to 09.00 h, using an automatic video camera. During the nest-building and egg-laying stages, focal individuals of some pairs with auxiliary birds, mainly females, were tracked and interactions with other group members were recorded. Casual data about antipredator behaviour and territorial defence were also collected during nest searches and censuses. Data from 1994 to 1997 were used for the analyses of the contributions of auxiliary birds, because most observations were made during this period. Some groups varied in size from one year to the next. Thus a pair might have more than one bird helping them in one year, but none the next. We compared the reproductive success of such pairs between years with and without auxiliaries. It was not possible to evaluate the quality of each territory directly. In order to determine whether pairs in particular territories, even without auxiliary birds, had higher fledging success than pairs in different territories, we compared the mean number of fledglings reared by pairs without helpers among pairs differently categorized based on the number of years in which they bred with auxiliary. Pairs breeding alone each year (called single pairs ) were compared with pairs breeding with auxiliary birds for 2 years or more ( temporary single pairs ). Only data from groups studied for at least 3 years were used in the analysis. Results GROUP COMPOSITION AND DISPERSAL OF YOUNG Pairs unaccompanied by auxiliary individuals comprised more than half of all the groups studied (see Table 1). Pairs with one to four auxiliaries comprised 24 43% of all breeding groups. Almost all auxiliaries were 1 year old or older males. Auxiliary females were observed in only five groups during the breeding season. The proportion of males more than 1 year old among the auxiliary males varied from year to year by 33% to 62%. Based on the genealogical data available from ringing, most auxiliaries were offspring that had remained in their natal territory. Most 1-year-old females emigrated from the study area by the beginning of each breeding season (see Table 2). Ten 1-year-old females remained within the study area, seven of which bred but not in their natal territories. In contrast, males were philopatric and none of 44 surviving 1-year-old males bred (Table 2). Among the 26 auxiliary 1-year-old males for which behavioural data were obtained, 13 helped breeding pairs in nest-building and/or feeding chicks (Table 2). Of four such males that dispersed from their natal territories, three became non-breeding auxiliaries in nonnatal groups and one became a floater. Of these 44 males, 29 survived into subsequent years, of which 16 remained as non-breeding auxiliaries in their natal territories, four as non-breeding auxiliaries in non-natal territories and nine were successful in attracting mates. Table 1. Composition of rufous vanga breeding groups. Only groups of which all members were identified are shown. From 1995 onwards the study area was enlarged 1994 1995 1996 1997 1998 1999 Pairs 8 17 25 23 38 26 Pairs with female(s) 0 0 1 1 0 0 Pairs with 1-year male(s) 2 5 7 9 1 4 6 Pairs with adult male(s) 3 1 7 5 2 5 7 9 Pairs with adult and 1-year males 1 1 1 5 1 2 Total 14 31 39 43 50 43 1 Including one group with one auxiliary female that provided no help. 2 Including one group with two auxiliary females that provided no help.

126 K. Eguchi et al. Table 2. Status of surviving yearling rufous vangas. Data from 1994 to 1999 combined Philopatric Dispersed Helper Non-helper Unknown Bred Non-breeder Male 13 13 14 0 4 1 Female 0 3 0 7 18 2 1 Three moved to nonparental territories and stayed there; one became a floater. 2 All emigrated from the study area by the beginning of the breeding season. Table 3. Pattern of independence of auxiliary male rufous vangas Two years old Three years old or older Total 12 9 Replaced in the same territory 0 1 Adjacent territory Newly established 8 6 Takeover 1 0 Spaced one territory distance Newly established 2 0 Takeover 0 1 Floater or not stable 1 1 Among auxiliary males that achieved independence, most established their own territories adjacent to the territory in which they had spent the previous year as a helping or non-helping auxiliary (Table 3). This tendency did not differ between 2-year-old and older males. HELPING BEHAVIOURS Auxiliary 1-year-old or older males helped breeding pairs in antipredator aggression, in territorial defence and by provisioning chicks (see Fig. 1). Auxiliary birds participated in about 60% of all antipredator defence events observed (Fig. 1a), and in about 80% of incidences of territorial defence (Fig. 1b). In most cases, all members of a group that were present participated in chasing predators and in territorial defence. This may indicate that all group members were exposed to the same risk. In terms of provisioning of chicks, auxiliary birds contributed about 25%, an amount very similar to that of breeding females (Fig. 1c). In about one-third of the groups (12 5 50 0%) for which nest watches were conducted, however, auxiliary birds did not provision chicks at all. In other groups with more than one auxiliary, only some auxiliaries contributed. Hence, the variation in provisioning behaviour among auxiliary males was very great, ranging from nil to about 40%. Some auxiliary birds also tried to help in nest-building and incubation, but the frequency was very low, sharing only 4% (1-year-old males) and 5% (older males) of nest material carrying, and 1% (1-year-old males) Fig. 1. Contribution of group members to: (a) percentage of participation in antipredator defence (27 groups), (b) percentage of participation in territorial defence (20 groups) and (c) percentage of contribution to provisioning of chicks after day 8. M = breeding males; F = breeding females; aux = auxiliaries. Vertical bars indicate SE. Values above error bars are numbers of individuals observed. Data were combined for 4 years from 1994 to 1997. and 10% (older males) of incubation. Older auxiliary males often carried nest materials and visited nests for incubation, but were usually attacked by breeding males. During the nest-building and egg-laying stages, breeding males often attacked older auxiliary males, but the aggression ceased thereafter (Table 4), indicating that breeding males preferred to prevent

127 Cooperative breeding in rufous vanga Table 4. The change in frequency of attacks by breeding males against auxiliary birds in relation to the stage of the breeding season (data from 1995 to 1997). Figures indicate the number of attacks/observation time (min) Breedingstage One-year-old males Two years or older Nest-building 4/941 108/6769 Egg-laying 0/1196 51/5749 Incubation 0/4385 7/8018 Nestling 0/16514 1/8595 auxiliaries from helping during the earlier stages of breeding. Attacks against 1-year-old males were rare. Of 11 such helping males, seven remained in the same territory in the following year, while eight of 10 non-helping 1-year-old males did (P = 0 635, Fisher s exact probability test), indicating that breeders did not expel nonhelping auxiliaries. Survival of 1-year-old auxiliary males did not differ between those that helped and those that did not [78 9% (n = 19) vs. 71 4% (n = 14); P = 0 695, Fisher s exact probability test], indicating that provisioning is not costly in this species. BREEDING SUCCESS The proportion of successful groups fledging at least one chick varied from year to year, ranging from 21% to 63%. If they failed, replacement nests were built; four replacement nests at most being built. Brood reduction was unusual, occurring in only 12 of 69 nests (17 4%) in which broods survived after day 10. The major causes of failure were: desertion during nest-building, and total loss of clutches or broods after egg-laying, probably as a result of predation (Table 5). We were unable to determine which predators were involved in most cases, but lemurs, snakes and birds of prey were often mobbed by rufous vangas when they were near their nests. RELATIONSHIP BETWEEN GROUP SIZE AND REPRODUCTIVE SUCCESS When the data from all years were combined, pairs with auxiliary birds were found to be significantly more successful as breeders than those without [45% (31/69) for pairs with auxiliary birds, and 30% (35/118) for those without, P = 0 0401, Fisher s exact probability test]. Furthermore, groups with auxiliary birds fledged more chicks than those without [1 19 ± 1 53 (n = 69) vs. 0 62 ± 1 11 (n = 117), U = 3272, P = 0 0116, Mann Whitney U-test]. Pairs that received provisioning assistance for their chicks from auxiliary birds succeeded in fledging more young than those without provisioning help [84% (21/ 25) vs. 55% (40/73); P = 0 0094, Fisher s exact probability test]. The number of fledglings was also significantly larger among the former than the latter [2 08 ± 1 41 (n = 25) vs. 1 19 ± 1 33 (n = 72); U = 576, P = 0 0056, Mann Whitney U-test]. Further analysis of pairs with auxiliary birds that successfully fledged young, provisioning by auxiliary birds made no significant difference [84% (21/25) for pairs in which auxiliary birds provisioned and 75% (6/8) for those in which auxiliary birds did not provision; P = 0 6162, Fisher s exact probability test]. Neither did the number of fledglings differ significantly between them [2 08 ± 1 41 (n = 25) for groups with helping auxiliaries and 1 88 ± 1 46 (n = 8) for those with non-helping auxiliaries; U = 91 5, P = 0 7154, Mann Whitney U-test]. Neither the presence of auxiliary birds nor brood size affected the body weight of nestlings between days 10 and 16 (P > 0 70, ANCOVA), nor hastened fledging. Fledging occurred after 15 7 ± 1 18 days (n = 18) for groups with provisioning auxiliaries and after 15 6 ± 1 26 days (n = 28) for those without (U = 239, P = 0 778, Mann Whitney U-test). Table 5. Causes of nesting failure. Figures indicate the number of nests 1994 1995 1996 1997 1998 1999 All nests built 26 47 50 79 78 68 First nests 13 31 33 43 46 39 Replacement nests 13 16 17 36 32 29 Successful 5 15 17 9 10 10 Failed Before egg-laying 8 8 9 25 8 8 Deserted 7 6 9 20 6 5 Destroyed 1 2 0 4 2 3 Unknown 0 0 0 1 0 Egg failure 6 8 7 34 39 39 Disappeared gradually 0 0 0 0 2 3 Disappeared totally 6 8 7 34 37 36 Nestling failure 2 9 11 11 18 10 Disappeared gradually 0 0 0 0 1 4 Disappeared totally 2 9 11 11 17 6 Unknown 5 7 6 0 4 1

128 K. Eguchi et al. COMPARISON OF REPRODUCTIVE SUCCESS BETWEEN YEARS FOR THE SAME PAIRS WITH DIFFERENT GROUP SIZES The apparent effect of the presence of auxiliary birds on the reproductive success of pairs shown above may in fact be brought about by confounding factors other than helping. We compared the number of fledglings produced by the same pairs between years when they were unaccompanied by auxiliaries and those years when they were accompanied (1 55 ± 1 15 vs. 1 39 ± 1 72, n = 18), and found that there was no significant difference between them (P = 0 590, Wilcoxon paired rank test). This means that it was not the presence of auxiliary birds that affected reproductive success. Moreover, temporary single pairs fledged more chicks than single pairs, even in the years when they bred without auxiliary birds [1 47 ± 1 15 (n = 18) vs. 0 52 ± 1 15 (n = 12); U = 52 5, P = 0 017, Mann Whitney U-test]. This means that certain pairs tended to have higher fledging success than others, even without help. Discussion GROUP COMPOSITION AND AUXILIARY BIRDS In the rufous vanga, females usually disperse from their natal territory by their first breeding season and some of them obtain a mate. In contrast, few young males disperse from their natal territory. One-year-old males are subordinate to older males and are not sexually mature (S. Yamagishi, unpublished data). Once they are sexually mature, they disperse and may obtain breeding status; some, however, remain with their parents for several years. In all cases but one, males dispersed alone. In most cases of independence, males established their own territories adjacent to the territory in which they had spent the previous year, which in most cases was their natal territory. Males may therefore have enhanced their chances of acquiring a territory by means of remaining within their natal territory. Once they have established a territory, they maintain it for many years. Of 13 breeding male rufous vangas banded in 1994, eight had maintained their dominant status for at least 6 years and one for 5 years. Such a pattern of independence by subordinate males has also been found among Florida scrub jays Aphelocoma c. coerulescens Bosc (Woolfenden & Fitzpatrick 1984). Dominant females changed their breeding groups more frequently than did males, the mean length of tenure being 5 1 years for males and 2 4 years for females, based on data from eight territories in Jardin A during the 6-year study. As a result of their movements, breeding females were often unrelated to their helpers. In such a situation, remaining in their natal territory may provide adult auxiliary males with a chance of mating with their stepmothers. Because auxiliary males are usually the sons of breeding males the sharing of alleles was very high, making it difficult to demonstrate the paternity of auxiliary males. Nevertheless, in at least one case an adult auxiliary male is known to have sired chicks (S. Yamagishi, unpublished data). Within the original Jardin A study area (550 450 m), where studies were begun in 1994, four territories disappeared and a total of eight new territories were established during the 6-year study period. Thus, the habitat in this area may not have been fully saturated. However, there were no solitary 1-year-old individuals in the study area, which suggests that belonging to a group may be necessary for survival, probably because floaters are harassed by territory owners. Because 1- year-old males are not sexually mature, they are unable to obtain mates. It seems that remaining in the natal territory is the most effective behaviour for them. These various observations indicate that the delayed dispersal of 1-year-old male rufous vangas matches the predictions of the benefits-of-philopatry hypothesis (Stacey & Ligon 1991). THE EFFECTS OF HELPING In many cooperative breeding species, the existence of auxiliary individuals apparently enhances the reproductive success of breeding pairs (Brown 1987; Stacey & Koenig 1990; Emlen 1991). However, confounding factors other than group size may affect the reproductive success (Emlen 1991; Cockburn 1998). In this study, the proportion of successful breeding attempts was higher in the groups with auxiliary birds than in those without them. However, higher probability of successful breeding was contributed by the high reproductive success of particular groups. Thus, large group size was a result, not a cause, of high reproductive success of particular groups as Emlen (1991) suggested. Hence, in the rufous vanga, although the contribution to breeding by auxiliary birds was remarkable, no effect of helping was found. This result is similar to those found in the white-browed scrubwren Sericornis f. frontalis (Vigors & Horsfield) (Magrath & Yezerinac 1997) and the kookaburra Dacelo novaeguineae Hermann (Legge 2000). The quality of the territory and/or of the breeding pair might affect both the number of auxiliaries attracted or retained and overall reproductive success. Unfortunately, we were unable to determine which factor is most plausible, because few data were available from different pairs occupying the same territory in different years. Because most breeding failures were due to predation, pairs in territories safe from predators may have a higher probability of breeding successfully. Predators were only observed on a few occasions during nest watches and censuses, making it difficult to compare the risk of predation among different territories. When considering other fitness-related parameters than reproductive success, the effects of provisioning

129 Cooperative breeding in rufous vanga by helpers were ambiguous. Under conditions of high nest predation, rapid nestling growth is advantageous. Provisioning by auxiliary birds, however, neither facilitated the growth of nestlings nor shortened the nestling period during which they are particularly vulnerable. Because the rufous vanga is long-lived, we have not been able to examine during the 6-year study whether the presence of helpers increases the survival of breeders. In those groups where auxiliary birds helped to provision chicks, the breeding female s provisioning rate was significantly lower than in groups without help; however, the breeding male s provisioning rate did not vary (K. Eguchi, unpublished data). Thus, helping may reduce parenting costs, at least for females. Breeding females, however, were often unrelated to their helpers, thus even if helping increases the survival of breeding females, it does not always enhance the inclusive fitness of helpers. WHY DO AUXILIARIES HELP? The reason why 1-year-old males do not disperse from their natal territory is clear. However, the reason why they help is not clear. Emlen (1991) and Cockburn (1998) have listed the various hypotheses explaining helping behaviour. These hypotheses fall into four categories on the basis of the operating mechanism of helping; (1) enhancement of current reproductive success; (2) enhancement of the survival of the breeders; (3) acquisition of skills for breeding; and (4) advertisement of helping behaviour. In the first case, enhancing current reproductive success, helpers can expect both direct and indirect benefits. If helpers assist kin, then enhancement of current reproductive success increases their own inclusive fitness. Inclusive fitness is also enhanced through increasing the survival of breeders. Helpers may gain skills for breeding during their investment. Finally, helpers may advertise their helping behaviour thereby enhancing their probability of being chosen as a mate (Emlen 1991; Boland et al. 1997), or of being allowed to remain in a territory (payment as rent). In this study, neither increased group size nor help by auxiliaries increased the reproductive success or survival of breeding pairs. Therefore, auxiliary birds gained neither direct benefits nor inclusive fitness through the enhancement of current reproductive success and/or survival of breeders. Helping behaviour might be beneficial to helpers even if it does not enhance the reproductive success of breeding pairs. If helping is payment for staying in a territory, then non-helping males might be expected to be expelled by breeders. However, breeders did not expel non-helping auxiliaries, although breeding males often attacked adult auxiliary males visiting a nest for nest-building or incubating. Thus breeding males do not always force auxiliary males to help them. The extent of provisioning by auxiliary birds varied greatly among individuals. If the probability that auxiliary males sired chicks was high, then they could be expected to provision at a high rate (Davies 1992). Among white-browed scrubwrens, auxiliary males provision nestlings more when the breeding females are unrelated to them (Magrath & Whittingham 1997). In the rufous vanga, the provisioning rate did not differ between auxiliary males that were related to breeding females and those that were unrelated; furthermore, the provisioning rate of the auxiliary male known to have sired chicks was not particularly high (K. Eguchi, unpublished data). Our data are too scarce to demonstrate a relationship between paternity and provisioning rate of auxiliary males. Auxiliary birds often participated in antipredator defence and territorial defence. Participation of auxiliary birds in defence against predators and conspecific birds may be more or less useful for breeding pairs. The fact that brood reduction was rare suggests that food resources were not short. If so, breeding pairs may allow auxiliary birds to stay in their territory, even if auxiliary birds do not feed chicks at all. Ligon & Stacey (1989) suggested that because alloparental provisioning by helpers may be derived from a general stimulus response behaviour to begging chicks, and because selection pressures on helpers provisioning may be different from species to species, in some species no adaptive function of helping is evident. In the rufous vanga, the large variation in the provisioning rate among auxiliary birds did not translate into any measurable differences in fitness-related values. Also, breeding pairs did not always accept help; in fact they often chased auxiliary birds carrying nest material or food away from their nest. These facts perhaps indicate that helping behaviour in this species lacks functional significance in spite of the high level of helping exhibited by some individuals. Indeed, we were unable to demonstrate any effects of helping for breeding pairs. In some species, helping is costly to young birds (Heinsohn & Cockburn 1994; Heinsohn & Legge 1999). However, provisioning may not be so costly in the rufous vanga because survival did not differ between 1-year-old auxiliary males that helped and those that did not. If it is not a costly activity, then provisioning by auxiliary birds may prevail even if its benefits are not so large. However, our data on helpers direct benefits from helping are limited. Auxiliaries may gain parenting skills through their helping behaviour. Data on this hypothesis are insufficient because our study was too short to clarify whether the experience of helping increased the reproductive success of past helpers after their independence. Further study of this subject may provide interesting answers to this and other questions. Acknowledgements We are grateful to the Government of the Republic of Madagascar for providing permission to conduct

130 K. Eguchi et al. research in the nature reserves, and to Dr Albert Randrianjafy, Director of Park Botanique et Zoologique de Tsimbazaza and staff members J. R. Ramanampamonjy, H. Randriamahazo, F. Rakotondraparany, B. Raveloson and J. Razanatsoa, for their kind co-operation during the study. T. Mizuta, M. Hotta, M. Tanimura, T. Masuda, F. Iwasaki, H. E. Amano, S. Fukushima and Y. Takeda assisted in fieldwork. We are also grateful to Dr S. M. Goodman for valuable information and advice; two anonymous referees for their valuable suggestions and Dr M. Brazil for improvements to the final draft. We also thank the staff of Conservation International for lodging and facilities at the Forest Station and H. Matsukawa, Embassy of Japan, for various support. This study was supported partly by a Grant-in-Aid from the Monbusho International Scientific Research Program (no. 06041093). References Appert, O. (1970) Zur Biologie der Vangawurger (Vangidae) sudwest Madagaskars. Ornithologische Beobachter, 67, 101 133. Boland, C.R.J., Heinsohn, R. & Cockburn, A. (1997) Deception by helpers in co-operatively breeding white-winged chough and its experimental manipulation. Behavioral Ecology and Sociobiology, 41, 251 256. Brown, J.L. (1987) Helping and Communal Breeding in Birds. Princeton University Press, Princeton. Cockburn, A. (1998) Evolution of helping behaviour in co-operatively breeding birds. Annual Review of Ecology and Systematics, 29, 141 177. Davies, N.B. (1992) Dunnock Behaviour and Social Evolution. Oxford University Press, Oxford. Eguchi, K., Nagata, H., Asai, S. & Yamagishi, S. (2001) Nesting habits of the rufous vanga in Madagascar. Ostrich, 72, 201 203. Emlen, S.T. (1991) Evolution of co-operative breeding in birds and mammals. Behavioural Ecology, an Evolutionary Approach, 3rd edn (eds J.R. Krebs, &. N.B. Davies), pp. 301 337. Blackwell, Oxford. Emlen, S.T. & Wregge, P. (1991) Breeding biology of white-fronted bee-eaters at Nakuru: the influence of helpers on breeder fitness. Ecology, 60, 309 326. Heinsohn, R. & Cockburn, A. (1994) Helping is costly to young birds in co-operatively breeding white-winged choughs. Proceedings of the Royal Society of London, B256, 293 298. Heinsohn, R. & Legge, S. (1999) The cost of helping. Trends in Ecology and Evolution, 14, 53 57. Innes, K.E. & Johnston, R.E. (1996) Cooperative breeding in the white-throated magpie-jay. How do auxiliaries influence nesting success? Animal Behaviour, 51, 519 533. Langrand, O. (1990) Guide to the Birds of Madagascar. Yale University Press, New Haven and London. Legge, S. (2000) The effect of helpers on reproductive success in the laughing kookaburra. Ecology, 69, 714 724. Leonard, M.L., Horn, A.G. & Eden, S.F. (1989) Does juvenile helping enhance reproductive success? A removal experiment on moorhens. Behavioral. Ecology and Sociobiology, 25, 357 361. Ligon, J.D. (1999) The Evolution of Avian Breeding Systems. Oxford University Press, Oxford. Ligon, J.D. & Stacey, P.B. (1989) On the significance of helping behavior in birds. Auk, 106, 700 705. Magrath, R.D. & Whittingham, L.A. (1997) Subordinate males are more likely to help if unrelated to the breeding female in co-operatively breeding white-browed scrubwrens. Behavioral Ecology and Sociobiology, 41, 185 192. Magrath, R.D. & Yezerinac, S.M. (1997) Facultative helping does not influence reproductive success or survival in cooperatively breeding white-browed scrubwrens. Journal of Animal Ecology, 66, 658 670. Razafy, F.L. (1987) La Réserve Forestière d Ampijoroa: Son Modéle et Son Bilan. Mémoire de fin d études. Université de Madagascar, Antananarivo. Stacey, P.B. & Koenig, W.D. (1990) Cooperative Breeding in Birds: long-term studies of ecology and behavior. Cambridge University Press, Cambridge. Stacey, P.B. & Ligon, J.D. (1991) The benefits-of-philopatry hypothesis for the evolution of co-operative breeding: variation in territory quality and group size effects. American Naturalist, 137, 831 846. Woolfenden, G.E. & Fitzpatrick, J.W. (1984) Florida Scrub Jays: demography of a cooperative-breeding bird. Princeton University Press, Princeton. Yamagishi, S. & Eguchi, K. (1996) Comparative foraging ecology of Madagascar vangids (Vangidae). Ibis, 138, 283 290. Yamagishi, S., Urano, E. & Eguchi, K. (1995) Group composition and contributions to breeding by rufous vangas Schetba rufa. Ibis, 137, 157 161. Received 11 June 2001; revision received 4 October 2001