Mark T. Stanback

The Evolution of Delayed Dispersal in Cooperative Breeders

Why do the young of cooperative breeders-species in which more than two individuals help raise offspring at a single nest-delay dispersal and live in groups? Answering this deceptively simple question involves examining the costs and benefits of three alternative strategies: (1) dispersal and attempting to breed, (2) dispersal and floating, and (3) delayed dispersal and helping. If, all other things being equal, the fitness of individuals that delay dispersal is greater than the fitness of individuals that disperse and freed on their own, intrinsic benefits are paramount to the current maintenance of delayed dispersal. Intrinsic benefits are directly due to living with others and may include enhanced foraging efficienty and redudec susceptibility to predation. However, if individuals that disperse and attempt to breed in high-quality habitat achieve the highest fitness, extrinsic constraints on the ability of offspring to obtain such high-quality breeding opportunities force offspring to either delay dispersal or float. The relevant constraint to independent reproduction has frequently been termed habitat saturation. This concept, of itself, fails to explain the evolution of delayed dispersal. Instead, we propose the delayed-dispersal threshold model as a guide for organizing and evaluating the ecological factors potentially responsible for this phenomenon. We identify five parameters critical to the probability of delayed dispersal: relative population desnity, the fitness differential between early dispersal/breeding and delayed dispersal, the observed or hypothetical fitness of floaters, the distribution of territory quality, and spatiotemporal environmental variability. A key conclusion from the model is that no one factor by itself causes delayed dispersal and cooperative breeding. However, a difference in the dispersal patterns between two closely related species or populations (or between individuals in the same population in different years) may be attributable to one or a small set of factors. Much remains to be done to pinpoint the relative importance of different ecological factors in promoting delayed dispersal. This is underscored by our current inability to explain satisfactory several patterns including the relative significance of flooting, geographic biases in the incidence of cooperative breeding, sexual asymmetries in delayed dispersal, the relationship between delayed dispersal leading to helping behavior and cooperative polygamy, and the rarity of the co-occurrence of helpers and floaters within the same population. Advances in this field remain to be made along several fronts. In particular, we advocate experimental tests of specific ecological factors affecting the parameters of the delayed-dispersal threshold model, studies of noncooperatively breeding taxa focusing on what constraints to independent reproduction exist and why they do not result in delayed dispersal, and studies of intraspecific variation in group size and composition of cooperative breeders in relation to local habitat gradients and patchiness.

NATAL DISPERSAL IN THE COOPERATIVELY BREEDING ACORN WOODPECKER

Abstract Dispersal data are inevitably biased toward short-distance events, often highly so. We illustrate this problem using our long-term study of Acorn Woodpeckers (Melanerpes formicivorus) in central coastal California. Estimating the proportion of birds disappearing from the study area and correcting for detectability within the maximum observable distance are the first steps toward achieving a realistic estimate of dispersal distributions. Unfortunately, there is generally no objective way to determine the fates of birds not accounted for by these procedures, much less estimating the distances they may have moved. Estimated mean and root-mean-square dispersal distances range from 0.22–2.90 km for males and 0.53–9.57 km for females depending on what assumptions and corrections are made. Three field methods used to help correct for bias beyond the limits of normal study areas include surveying alternative study sites, expanding the study site (super study sites), and radio-tracking dispersers within a population. All of these methods have their limitations or can only be used in special cases. New technologies may help alleviate this problem in the near future. Until then, we urge caution in interpreting observed dispersal data from all but the most isolated of avian populations.

Reproductive roles in the cooperatively breeding acorn woodpecker: incest avoidance versus reproductive competition.

Incest is rare in the cooperatively breeding acorn woodpecker (Melanerpes formicivorus) despite a polygynandrous mating system in which nearly all group members are close relatives. Here we test the relative importance of avoiding matings between close relatives (incest avoidance) and within‐sex competition for breeding opportunities (reproductive competition) in determining the mating system of acorn woodpeckers by examining how reproductive roles change following breeding vacancies. In 83% of cases in which helpers of the same sex were present in the group, reproductive vacancies were resolved when new unrelated immigrants filled the vacancy to the exclusion of resident same‐sex helpers, who generally emigrated or did not breed while they remained in the group. Helpers of the opposite sex, especially when male, were significantly more likely to remain in their natal group and in about half the cases inherited and bred following reproductive vacancies. This result was not explainable by reproductive competition, since the number of immigrants was often less than or equal to the number of same‐sex helpers in the group. Apparent incest resulted in 5% of cases. The time required to resolve reproductive vacancies was significantly longer for groups with helpers of the same sex as the vacancy. These results confirm that both incest avoidance and reproductive competition are important factors determining reproductive roles within groups of this highly social species.

NEST-SITE SELECTION IN THE ACORN WOODPECKER

Acorn Woodpeckers (Melanerpes formicivorus) at Hastings Reservation in central California prefer to nest in dead limbs in large, dead valley oaks (Quercus lobata) and California sycamores (Platanus racemosa) that are also frequently used as acorn storage trees. Based on 232 nest cavities used over an 18-year period, we tested whether preferred or modal nest-site characters were associated with increased reproductive success (the nest-site quality hypothesis). We also examined whether more successful nests were likely to experience more favorable microclimatic conditions or to be less accessible to terrestrial predators. We found only equivocal support for the nest-site quality hypothesis: only 1 of 5 preferred characters and 2 of 10 characters exhibiting a clear modality were correlated with higher reproductive success. All three characteristics of nests known or likely to be associated with a more favorable microclimate, and two of five characteristics likely to render nests less accessible to predators, were correlated with higher reproductive success. These results suggest that nest cavities in this population are built in part to take advantage of favorable microclimatic conditions and, to a lesser extent, to reduce access to predators. However, despite benefits of particular nest characteristics, birds frequently nested in apparently suboptimal cavities. We also found a significant relationship between mean group size and the history of occupancy of particular territories and the probability of nest cavities being built in microclimatically favorable live limbs, suggesting that larger groups residing on more stable territories were better able to construct nests with optimal characteristics. This indicates that there may be demographic, as well as ecological, constraints on nest-site selection in this primary cavity nester.

Patterns and consequences of egg destruction among joint-nesting acorn woodpeckers

Reproductive competition among joint-nesting female acorn woodpeckers, Melanerpes formicivorus, culminates in the removal and subsequent destruction of eggs laid by co-breeders. Females destroying eggs gain both by synchronizing egg laying and by having more of their own eggs incubated in the final clutch. Here results are summarized based on observations of 19 joint nests. Egg destruction accounted for the loss of 38% of all eggs laid. Either or both joint-nesting females destroyed eggs at the same nest, and a female that destroyed eggs during one nesting attempt sometimes had her own eggs destroyed during the next. Egg destruction was not moderated by the genetic relatedness of joint-nesting females and was apparently unrelated to behavioural dominance, but substantially lowered per female success of three- compared with two-female nests. Females did not discriminate between eggs; thus egg destruction ended when both females laid normal eggs simultaneously in the nest cavity. However, egg destruction ended most frequently when a female did not destroy an egg laid by her co-breeder 1 day prior to laying her own first egg. Such failures to destroy eggs entail short-term fitness costs that may be compensated by the potential for reciprocity across breeding attempts. Abnormally small ‘runt’ eggs, rarely found in other species of birds, were commonly laid as the first egg of the clutches of one or both joint-nesting females. The laying of runt eggs may allow females to destroy normal eggs laid simultaneously by their co-breeders. Egg destruction is a major constraint on the degree to which females nest jointly. More generally, egg destruction and its associated behaviour patterns demonstrate that reproductive interference can be as complex and destructive within groups of close relatives as between unrelated individuals.

Shared parentage and incest avoidance in the cooperatively breeding acorn woodpecker

Social groups of acorn woodpeckers (Melanerpesformicivorus) range in size from unaided pairs to 15 adults. Behavioural indicators of mate guarding, assumed incest avoidance and observations of egg‐laying indicate that social organization ranges from monogamous pairs to groups with up to seven male and three female putative cobreeders plus up to 10 nonbreeding helpers. In addition, groups occasionally lack a putative breeder throughout the breeding season. Here we report results from multilocus DNA fingerprinting of 372 nestlings from 123 nests in groups with putative cobreeders of one or both sexes. No extra‐group fertilizations were found. Putative cobreeding males within social groups shared paternity. However, the most reproductively successful male was, on average, almost three times as successful as the next most successful and additional males only occasionally sired offspring. In contrast, cobreeding females shared parentage equally. Helpers never bred incestuously when their opposite‐sex parent (or another relative, such as their uncle) held breeding status in the group. However, during breeding male vacancies, 14 nestlings were produced when helper males bred incestuously with their mother. Both male and female helpers usually became successful cobreeders with their same‐sex parent following replacement of the opposite‐sex breeder(s) by unrelated individuals.

Within-season Nest-site Fidelity in Eastern Bluebirds: Disentangling Effects of Nest Success and Parasite Avoidance

Abstract We manipulated nestbox choices in Eastern Bluebirds (Sialia sialis) to assess (1) whether the presence of a previously used (and presumably parasite-ridden) nest cavity increases or decreases the likelihood of within-season nestbox reuse and (2) whether birds prefer previously successful cavities. Initially, birds were presented with two clean identical nestboxes erected 1 m apart. After the first nesting, we removed nest material from half of the successful box pairs and recorded subsequent nesting choices. Given a choice between a used and an unused box, bluebirds chose the unused but parasite-free cavity significantly more often. Presented with a cleaned successful box and an identical unused one, bluebirds opted to reuse the former significantly more often. Those results suggest that (1) bluebirds recognize a cost of within-season nest reuse and are willing to switch nest sites to minimize parasitism, (2) bluebirds prefer successful cavities, but only if they are clean, and (3) in our population, in which cost of nest switching was minimized, the aversion to parasites was stronger than the preference for successful cavities.

Spatiotemporal Patterns in Nest Box Occupancy by Tree Swallows Across North America

Data from the North American Breeding Bird Survey (BBS) suggest that populations of aerial insectivorous birds are declining, particularly in northeastern regions of the continent, and particularly since the mid-1980s. Species that use nest boxes, such as Tree Swallows (Tachycineta bicolor), may provide researchers with large data sets that better reveal finer-scale geographical patterns in population trends. We analyzed trends in occupancy rates for ca. 40,000 Tree Swallow nest-box-years from 16 sites across North America. The earliest site has been studied intensively since 1969 and the latest site since 2004. Nest box occupancy rates declined significantly at five of six (83%) sites east of -78° W longitude, whereas occupancy rates increased significantly at four of ten sites (40%) west of -78° W longitude. Decreasing box occupancy trends from the northeast were broadly consistent with aspects of a previous analysis of BBS data for Tree Swallows, but our finding of instances of increases in other parts of the continent are novel. Several questions remain, particularly with respect to causes of these broadscale geographic changes in population densities of Tree Swallows. The broad geographic patterns are consistent with a hypothesis of widespread changes in climate on wintering, migratory, or breeding areas that in turn may differentially affect populations of aerial insects, but other explanations are possible. It is also unclear whether these changes in occupancy rates reflect an increase or decrease in overall populations of Tree Swallows. Regardless, important conservation steps will be to unravel causes of changing populations of aerial insectivores in North America. RESUME. Les donnees provenant du Releve des oiseaux nicheurs (BBS) de l’Amerique du Nord semblent indiquer que les populations d’insectivores aeriens sont en declin, particulierement dans les regions du nord-est du continent et depuis le milieu des annees 1980. Grâce aux especes qui utilisent les nichoirs, comme l’Hirondelle bicolore (Tachycineta bicolor), les chercheurs ont acces a une grande quantite de donnees qui revelent davantage les tendances des populations a l’echelle fine. Nous avons analyse la tendance du taux d’occupation par l’Hirondelle bicolore a partir de 40 000 nichoirs-annees provenant de 16 sites repartis en Amerique du Nord. Le site le plus ancien est suivi intensivement depuis 1969 et le plus recent, depuis 2004. Le taux d’occupation des nichoirs a diminue significativement dans 5 des 6 sites (83 %) situes a l’est du 78° de longitude ouest, tandis qu’il a augmente significativement dans 4 des 10 sites (40 %) a l’ouest du 78° de longitude ouest. La tendance a la baisse de l’occupation observee dans le nord-est concorde dans les grandes lignes avec les resultats d’une analyse anterieure des donnees du BBS pour cette espece, mais les hausses que nous avons observees dans d’autres regions de l’Amerique du Nord s’averent nouvelles. Plusieurs interrogations demeurent, notamment en ce qui a trait aux causes de ces changements dans la densite des populations d’Hirondelles bicolores a grande echelle. Ces vastes tendances geographiques concordent avec l’hypothese de changements climatiques generalises qui toucheraient les aires d’hivernage, de migration ou de nidification, lesquels pourraient affecter differemment les populations d’insectes aeriens, mais d’autres explications sont aussi possibles. En outre, nous ne savons pas si ces changements du taux d’occupation refletent une hausse ou une baisse dans l’ensemble des populations d’Hirondelles bicolores. Neanmoins, pour assurer leur conservation, il sera important d’elucider les causes des changements de populations chez les insectivores aeriens en Amerique du Nord.

Demographic consequences of incest avoidance in the cooperatively breeding acorn woodpecker.

The avoidance of breeding with close relatives is an adaptation to inbreeding depression. Unfortunately, inbreeding depression has proved difficult to document or measure in the wild, despite being frequently observed among animals in captivity. We address this problem indirectly by determining the demographic cost of incest avoidance in the cooperatively breeding, polygynandrous acorn woodpecker, Melanerpes formicivorus, following the death or disappearance of all breeders of one sex within a group (a reproductive vacancy). Groups undergoing female vacancies that also contained female nonbreeding helpers experienced significantly lower reproductive success in each of the subsequent 3 years than those in which either no nonbreeding helpers or only male nonbreeding helpers were present, a decrease attributable to incest avoidance between the helper females and the related breeder males in the group. Using a computer simulation combined with a life-table analysis, we estimated that incest avoidance costs the population 9.2-12.1% in overall reproductive potential (measured in fledglings/female) and decreases the population rate of increase by 1.78-2.33%/year. These results suggest the presence, on average, of at least 1.2-1.8 lethal equivalents per individual, a value of the same magnitude as estimated for several other taxa, including humans. Incest avoidance may compound random demographic and environmental events and significantly facilitate the decline of threatened populations even prior to any detrimental effects of inbreeding depression per se. Copyright 1999 The Association for the Study of Animal Behaviour.

Genetic monogamy in single‐male groups of acorn woodpeckers, Melanerpes formicivorus

Acorn woodpeckers have one of the most complex social systems of any bird species. Breeding units range in size from monogamous pairs to groups of 15 birds that include multiple breeding males and females as well as nonreproductive helpers‐at‐the‐nest. Groups form when young remain at their natal nest to help their parents breed or when single‐sex coalitions of siblings disperse to fill a reproductive vacancy on another territory. Plural breeding and helping behaviour are thought to be favoured through indirect fitness benefits for individuals that would otherwise be unable to breed due to a shortage of reproductive vacancies on territories with acorn stores. We report the results of multi‐locus DNA fingerprinting of 51 offspring from 18 nests of 16 socially monogamous pairs of acorn woodpeckers. If socially monogamous females mate outside the pair‐bond, indirect fitness benefits for cobreeders and helpers will be significantly reduced. Monogamous pairs accounted for all but one of the 51 offspring we tested; the single exception was apparently sired by the putative father, but the putative mother was excluded from maternity. Our results indicate that individuals remaining on their natal territories as helpers are generally the genetic offspring of the pair they help. They also suggest that single‐sex coalitions offspring dispersing together from nests of socially monogamous pairs will be full‐siblings.