Peter H. Wrege

The role of kinship in helping decisions among white-fronted bee-eaters

SummaryWhite-fronted bee-eaters (Merops bullockoides) are cooperative breeders in which half of all nesting attempts are assisted by non-breeding adults in addition to the breeding pair. These “helpers” assist in all aspects of nesting and their aid significantly increases fledging success. The social unit in these bee-eaters is an extended family clan in which multiple pairs may breed simultaneously (plural breeding). As a result, helpers often have to choose how to allocate their aid among several potential recipients to whom they are unequally related. Using five years of data from a color-marked and genealogically known population of white-fronted bee-eaters in Kenya, we examined the role of kinship in three helping “decisions”: 1) whether or not to become a helper, 2) whom to help, and 3) how much help to provide.1)Kinship between potential donor and recipient was a significant predictor of the likelihood of helping. Fully 44% of the individuals that could have become helpers did not do so. Many of these non-helpers were unrelated mates (“in-laws”) that had paired into their partners clan and had no genetic link to the available recipients. Others were natal clan members with only distant genealogical ties to the breeders. The conditional probability of helping (see text for definition) decreased significantly with decreasing rh(coefficient of relatedness) between the potential helper and nestling recipients. The presumed cost of helping was a second significant predictor of whether or not a bird became a helper. We considered the expending of effort in providing aid and the delaying of personal reproduction to be costs of helping. Potential helpers that had engaged in high effort activities in the few weeks prior to the helping opportunity showed a decreased likelihood of becoming helpers. Similarly, paired birds (which by virtue of having a mating partner had a greater potential of breeding) were less likely to become helpers than were single individuals.2)Bee-eater helpers preferentially chose to aid their closest genetic relatives. The average relatedness between helpers and the nestlings receiving their aid was 0.33. This degree of kinship was significantly greater than that expected if helpers had selected recipient nests randomly from among those available within their clans. Further evidence of kin discrimination came from analysis of 115 instances in which a helper had two or more nests of differing relatedness simultaneously available as potential recipients. In 108 cases (94%), the helper aided the most closely related one.3)The magnitude of the helping contribution (as measured by provisioning rate) showed no pattern with relatedness between donor and recipient. These data allow testing of various theoretical models for the allocation of aid among kin. Since bee-eaters helped at only one nest at a time, and selected the nest with the most closely related young available, their behavior conforms to an allor-none case of a diminishing returns model and is inconsistent with alternative models based upon the distribution of aid in proportion to relatedness. We conclude that kinship is a major determinant in the decisions both of whether to become a helper, and of whom to help, in white-fronted bee-eaters.

BREEDING BIOLOGY OF WHITE-FRONTED BEE-EATERS AT NAKURU: THE INFLUENCE OF HELPERS ON BREEDER FITNESS

SUMMARY (1) Among white-fronted bee-eaters (Merops bullockoides) near Nakuru, Kenya, helpers dramatically increased the fitness of breeders. Using 5 years of data, we examine the relative importance of food availability, breeder attributes and group size on reproductive success. (2) Both food availability and size of the group attending the nest had significant effects on productivity, while the characteristics of breeders (age, experience) did not. Helpers had their effect almost entirely through increased productivity per nesting attempt, each helper on average increasing the number of fledglings by 0 50 (+0.06 S.E.). The activities of helpers did not affect either breeder survival or the number of nesting attempts per year. (3) The presence of helpers did not affect clutch size, had no influence on the probability of successful hatching, but dramatically increased the rate of provisioning per nestling. As a consequence of their feeding contributions, helpers significantly decreased both the probability of nestling starvation and the degree of nestling developmental retardation due to food stress. More young fledged, and fledged in better condition, from helped nests. (4) The mechanisms by which helpers have their effects are largely ecologically determined. The ability of bee-eater helpers to increase fledging success through their feeding contribution is related to the environmentally unpredictable, and often harsh, conditions at Nakuru. Nestling starvation rates were high (48% of all hatchlings), whereas predation losses were low (4% of eggs laid). In other, cooperative breeding species where helper feeding contributions have increased nestling growth and survival, sparse or unreliable food resources have also been the rule. In contrast, predation has been implicated as the major source of mortality in many other cooperative breeding species, and it is in these species that the anti-predator activities of helpers have been reported to have an important impact on nesting success. (5) Helper effects of the magnitude recorded in the Nakuru population of beeeaters are unusual. The presence of one helper effectively doubled the fledging success of an unaided pair, and the effect of increasing numbers of helpers was linear across all commonly observed group sizes. This large helper contribution has important implications for the behavioural options of both breeders and helpers. Not only should the presence/absence of helpers influence the decision to breed, but breeders are expected to compete for potential helpers. From the perspective of a potential

Biochemical determination of parental uncertainty in white-fronted bee-eaters

SummaryMaternity and paternity uncertainty represent important costs to breeders among white-fronted bee-eaters (Merops bullockoides) in Kenya. Analysis of enzyme polymorphisms reveals that between 9% and 12% of all offspring are genetically unrelated to one or both of their putative parents. These ‘bastards’ are the result of three different sources of parental uncertainty: Extrapair copulation, intraspecific egg parasitism, and quasi-parasitism (parasitism by a female who was fertilized by the male attending the parasitized nest). The first two represent costs to males, who rear offspring that are not genetically their own; the latter two produce the same costs for females. Genetic relatedness plays an important role in defining the social structure of M. bullockoides populations. In order to predict patterns of parental investment and the choice of recipients for helping behavior, one would like to know the relative frequency of maternity vs paternity uncertainty. The possible use of maximum likelihood techniques to separate the sources of non-kin is discussed. Unfortunately, the sample size of detected non-kin in the present study was not large enough to allow constructive use of the technique for bee-eaters. A comparison of estimates from biochemical and behavioral analyses indicates that both methods can produce misleading results. Behavioral data can be used to test underlying assumptions of biochemical analyses, and vice-versa. Used together, the two approaches reinforce one another and strengthen the reliability of conclusions drawn from either one alone.

BREEDING DISPERSAL AND PHILOPATRY IN THE TREE SWALLOW

Abstract To study the patterns and determinants of philopatry and breeding dispersal in the Tree Swallow (Tachycineta bicolor) we analyzed the records of 356 males and 1459 females captured in more than one breeding year around Ithaca, New York. Of these captures, only 4% of male and 14% of female breeders dispersed to a new site for breeding. With our combination of intensive study areas in Tompkins County, New York, and the efforts of volunteer banders throughout New York and surrounding states, we could have detected dispersal in excess of 400 km from the initial breeding site. Randomization tests revealed, however, that breeders dispersed much shorter distances than they could have been detected. Detailed analyses of recaptures in Tompkins County showed that over a 22-km range of distances, the chances of dispersal to a new breeding site declined with the distance from the original breeding site. Females that failed to fledge any offspring were much more likely to disperse than females that reproduced successfully, and the probability of dispersal declined gradually with female age. The spatial scale in which swallows gather and process information appears to be much larger than for passerines that defend all-purpose territories. Dispersión Reproductiva y Filopatría en Tachycineta bicolor Resumen. Para estudiar los patrones y los determinantes de la filopatría y la dispersión reproductiva en Tachycineta bicolor analizamos los registros de 356 machos y 1459 hembras capturados en más de un año reproductivo en los alrededores de Ithaca, New York. De estas capturas, sólo el 4% de los machos y el 14% de las hembras reproductivas se dispersaron a un nuevo sitio de cría. Con nuestra combinación de áreas de estudio intensivas en el Condado de Tompkins, New York, y los esfuerzos de colaboradores voluntarios que anillaron aves a lo largo de New York y los estados circundantes, pudimos haber detectado eventos de dispersión a más de 400 km desde el sitio de cría inicial. Exámenes aleatorizados revelaron, sin embargo, que las aves reproductivas se dispersaron a distancias mucho más cortas que las que se podrían haber detectado. Análisis detallados de recapturas en el Condado de Tompkins mostraron que en un rango de distancias de 22 km, las probabilidades de dispersión a un nuevo sitio de cría disminuyeron con la distancia desde el sitio de cría original. Las hembras que fracasaron en la cría de pichones presentaron una probabilidad de dispersarse mucho mayor que las hembras que se reprodujeron exitosamente, y la probabilidad de dispersión disminuyó gradualmente con la edad de la hembra. La escala espacial a la que T. bicolor recoge y procesa información parece ser mucho más grande que la de aves paserinas que defienden territorios de uso múltiple.

A test of alternate hypotheses for helping behavior in white-fronted bee-eaters of Kenya

SummaryConsiderable controversy exists over the question of the importance of kin selection in the maintenance of helping behaviors among birds. We examined nine different hypotheses of how helpers might benefit from engaging in alloparental care activities. We break these into four categories: Through its activities the helper may A) improve its probability of surviving to the following breeding season, B) enhance its probability of becoming a breeder in the future, C) increase its reproductive success when it does become a breeder, and D) increase the production of non-descendent kin. The first three categories provide direct fitness gains to the helper; in the fourth, the benefit is indirect. The hypotheses are not mutually exclusive; rather their fitness effects are additive. Each hypothesis, however, makes specific and often separable predictions about both 1) the type of fitness benefits expected, and 2) the characteristics of the birds that serve as helpers. We tested these predictions using five years data from a color marked and geneologically known population of white-fronted bee-eaters (Merops bullockoides) in Kenya. A) Survival was not related to status (breeder, helper, non-participant); nor did individuals living in large clans have better survival than those living in small ones. B) Newly formed pairs were equally likely to become future breeders irrespective of whether or not one or both individuals had helped previously. C) The mean number of young fledged by a first time breeder was unaffected by its prior helping experience. Neither were first time breeding pairs more likely to gain the services of others as their helpers than were pairs without prior helping experience. Taken together these results demonstrate that beeeaters gain very little direct benefit from alloparenting. D) Helpers did not enhance the survival of the breeders that they helped. But they did have a major effect in increasing nestling survival. Because bee-eater helpers are closely related to the nestlings they help to rear (average r=0.33), they obtain a large indirect benefit by increasing the production of non-descendent kin. We quantified the relative importance of indirect and direct benefits of helping (to the helper) using Vehrencamps “kin index”, Ik (1979). Ik compares the fitness consequences of helping against an alternative strategy and calculates the proportion of the inclusive fitness gain or loss that is due to kin (indirect) benefits. Comparing the strategy sets of helping versus not helping for bee-eaters, Ik=0.89 (indicating that 89% of the benefit derived from helping is indirect). When helping was compared against the alternative of breeding, Ik=2.17. Values of Ik greater than 1.0 indicate that direct fitness gains from the alternate strategy (breeding) are greater than those from helping. The value of 2.17 indicates that the helping strategy would not be maintained except for the indirect fitness gained through the increased production of close kin. Alloparenting in white-fronted bee-eaters can thus be considered as altruistic.

Flexible growth rates in nestling white-fronted bee-eaters : a possible adaptation to short-term food shortage

Nestling White-fronted Bee-eaters (Merops bullockoides) in Kenya show an ability to slow their development rate in response to food stress and, more importantly, to recover from stress with resumption of normal development. Successful fledging occurred at ages ranging from 22-42 days. The magnitude of developmental slowing was greatest: (1) among the youngest nestlings in large broods, (2) in seasons of overall low food availability, and (3) in nests provisioned by breeding pairs alone (i.e., nests without helpers). We speculate that this ability to slow growth reduces a nestlings daily energy requirements and thereby increases its likelihood of surviving through short periods of severe food shortage.

Size dimorphism, intrasexual competition, and sexual selection in wattled jacana (Jacana jacana), a sex-role-reversed shorebird in Panama

Abstract We studied sexual size dimorphism, intrasexual competition, and sexual selection in an individually marked population of Wattled Jacanas (Jacana jacana) in the Republic of Panama. Males are the sole incubators of eggs (28-day incubation) and primary providers of chick care (50–60 days). Females were 48% heavier than, and behaviorally dominant over, males. Females also showed greater development of secondary sexual characters (fleshy facial ornamentation and wing spurs) than males. Both sexes defended territories throughout the year against same-sex conspecifics. Competition for territorial space was intense, and many individuals of both sexes did not become breeders. Resident females further competed with one another to accumulate multiple mates, resulting in a mating system of simultaneous polyandry. Female and male residents (territory holders) were larger, heavier, and more ornamented than adult floaters of the same sex. Larger and heavier females also had more mates than smaller females. Body size was thus a critical predictor of success in intrasexual competition for territories (both sexes) and for mates (females). Three measures of sexual selection—(1) sex difference in the opportunity for sexual selection, (2) female-to-male ratio of potential reproductive rates, and (3) operational sex ratio—each indicated that sexual selection is currently operating more strongly on females than on males (female-to-male ratios ranged from 1.43:1 to 2.22:1). Values of 1.61:1 and 1.43:1 represent the first published quantitative estimates of the opportunity for sexual selection for any sex-role-reversed bird. Our study supports the theory that when increased parental care entails reduced opportunities for future reproduction, asymmetries in parental care behaviors of the sexes can influence the intensity of competition for mates and the direction and strength of sexual selection.

Cuckoldry as a cost of polyandry in the sex-role-reversed wattled jacana, Jacana jacana.

In this paper we provide the first molecular genetic data on extra–pair paternity in a simultaneously polyandrous, sex–role–reversed avian species, the wattled jacana (Jacana jacana). Female jacanas often copulated with multiple mates, provided that the mates were not actively incubating eggs or tending young chicks. Both the presence of multiple ‘available’ mates, and the copulation behaviour of the female near the time of nest initiation, significantly predicted the probability of extra–pair fertilizations. A males risk of being cuckolded was 0% in monandrous pairings, rose to 41% of broods (17% of chicks) in polyandrous associations where an additional mate was ‘available’, and increased to 74% of broods (29% of chicks) where the female was observed to copulate with multiple mates. Unlike findings from several sequentially polyandrous bird species, few if any fertilizations resulted from sperm stored from a previous nesting. We conclude that lost paternity can constitute a very real cost of polyandry for male wattled jacanas. The source of this cost is sexually active males simultaneously paired to the same female.

Niche expansion, body size, and survival in Galápagos marine iguanas

Abstract Foraging theory predicts that dietary niche breadth should expand as resource availability decreases. However, Galápagos marine iguanas often die during algae shortages (El Niños) although land plants abound where they rest and reproduce. On Seymour Norte island, a subpopulation of iguanas exhibited unique foraging behavior: they consistently included the succulent beach plant B. maritima in their diet. We investigated the consequences of land-plant feeding for body size and survival. Batis-eaters supplemented their algae diet both before and after intertidal zone foraging, and more Batis was eaten during tides unfavorable for intertidal zone foraging (dawn and dusk). Larger, energy-constrained iguanas fed more on land than did smaller animals. Compared to intertidal zone algae, Batis was 39% lower in caloric content (1.6 vs. 2.6 kcal g–1 dry mass), 56% lower in protein (8.3 vs. 18.9% dry mass) and 57% lower in nitrogen (1.3 vs. 3.0% dry mass). In spite of its lower nutrient value, iguanas that supplemented their diet with this plant were able to attain nearly twice the body size of other iguanas on the island. Age estimates indicate that many Batis-eaters survived repeated El Niño episodes during which animals of their relative size-class experienced high mortality on other islands. The larger animals were, however, completely dependent upon this supplementary source of food to maintain condition, and all perished in the 1997–1998 El Niño when high tides inundated and killed Batis on Seymour Norte Island. We hypothesize that Batis feeding developed as a local foraging tradition, and that dietary conservatism and strong foraging site fidelity explain why the inclusion of land plants in the diet has been observed in only a single population. Ultimately, a unique algae-adapted hindgut morphology and physiology may limit a switch from marine to terrestrial diet.

Breeding seasonality and reproductive success of white-fronted bee-eaters in Kenya

AssmAcT.-White-fronted Bee-eaters (Merops bullockoides) at Nakuru, Kenya, reproduce in an environment where food supply for provisioning nestlings is unpredictable and generally scarce. With data from 8 yr of study on three populations of bee-eaters, we examined how these environmental conditions have influenced the timing of breeding and patterns of nesting success. Breeding coincided with the general pattern of rainfall in the Rift Valley. Kenya experiences two rainy seasons per year, and individual bee-eaters bred with either the long or the short rains, but not both. Members of a given population bred colonially and quite synchronously, but members of adjacent populations were often out of phase with one another. As a result, the distribution of longand short-rains breeding populations formed a spatial mosaic. Reproductive success was highly variable but typically low. Mean (?SD) fledging success was 0.57 ? 0.83 young, and only one nest in four produced an independent offspring (6 months of age). Most prefledging mortality (88%) was due to egg losses and the starvation of young. Very little (7%) was attributable to predation. Social factors, primarily intraspecific nest parasitism, were responsible for nearly half of all egg losses, and represent an important cost of group living. Starvation, the single most important source of prefledging mortality, claimed the lives of 48% of all hatchlings. Starvation was greatest at times of low food availability, in nests with large broods, and in nests tended by pairs without helpers. Hatching was asynchronous. This enhanced the ability of older nestlings to monopolize limited food supplies, and resulted in the selective death of the smallest nestling first. Such brood reduction, coupled with the ability of nestlings to slow their development rate in response to food stress, is considered an adaptation for coping with the unpredictable variation in food supply commonly faced by these birds. Received 17 August 1990, accepted 18 January 1991.