Jeffrey R. Walters

The Determination of Clutch Size in Precocial Birds

The evolution and regulation of clutch size has long been a central issue in ornithology. Early ornithologists realized that females of each species of bird lay a characteristic number of eggs, and we have been trying to determine ever since why this is so. In pursuit of the answer to this seemingly simple question, ornithologists have not only accumulated a wealth of egg data, but also have made important contributions to such diverse topics as life-history strategies, population regulation and group selection. Yet how clutch size is determined remains a controversial issue. The consensus that was once sought in the form of a central theory (Lack, 1968; Cody, 1966; Klomp, 1970; von Haartman, 1971) has disappeared in a sea of specific hypotheses. In this review we attempt to organize and summarize clutch size theories as they emerge in modified form from recent research and evaluate their ability to explain observed patterns in clutch size variation. We concentrate on the literature and concepts published since the review of Klomp (1970), but we incorporate earlier work when necessary.

Test of the Ecological Basis of Cooperative Breeding in Red-Cockaded Woodpeckers

-In many cooperatively breeding birds, the primary reason that helpers remain on the natal territory rather than disperse to breed independently may be to gain an advantage in competing for high-quality habitat. We hypothesized that cavities excavated in living pines, because they require much time to construct, are the critical determinant of habitat quality that has led to cooperative breeding in Red-cockaded Woodpeckers (Picoides borealis). These woodpeckers rarely colonize sites that lack existing cavities. To test our hypothesis we drilled cavities in 20 unoccupied sites. Eighteen were occupied subsequently, but none of 20 control sites were used. The manipulation added 12 new social units (breeding pairs or unpaired territorial males) to the population. New groups mostly comprised previous helpers and dispersing first-year birds. These results support our contention that variation in habitat quality dependent on the presence or absence of cavities is the ecological basis of group formation in Red-cockaded Woodpeckers. Cavity construction may be used to increase the number of groups in a population, and to prevent territory abandonment when bird-constructed cavities are lost. Received 3 October 1990, accepted 24 June 1991. COOPERATIVE breeding refers to a social system found in birds and mammals in which some reproductively mature individuals (helpers) assist others in raising young (Brown 1978, 1987, Emlen and Vehrencamp 1983, Emlen 1992). Understanding the evolution of cooperative breeding involves two interrelated but distinct issues (Emlen 1982a, b, 1992, Brown 1985, 1987, Ligon and Stacey 1989): (1) determining what leads individuals to remain with their natal groups or form groups rather than disperse to breed independently; and (2) determining why such individuals engage in helping behavior such as feeding young. Altruism evolved through kin selection is an accepted explanation of helping behavior (issue 2; Emlen and Wrege 1988,1989). In contrast, remaining in the natal group (issue 1) and thereby delaying reproduction and altering dispersal behavior generally is viewed as producing direct benefits to the individual under certain conditions (Emlen 1982a, Woolfenden and Fitzpatrick 1984, Brown 1985, 1987, Stacey and Ligon 1987). Emlen (1982a) outlined two conditions under which remaining with the natal group may result in greater lifetime reproductive success than early dispersal and breeding. One condition involves a harsh, unpredictable environment. In I Present address: RD1, Box 27, Spring Mills, Pennsylvania 16875, USA. poor years, inexperienced birds reproduce poorly, so that living with the natal group is favored over independent reproduction. This hypothesis may apply to species that inhabit the dry regions of Africa and Australia (Reyer 1980, Emlen 1981, 1982a, Clarke 1984). The second, perhaps more common condition has traditionally been termed habitat saturation, because it is thought to result from a shortage of vacancies in breeding habitat (Selander 1964, Brown 1969, Stacey 1979, Emlen 1982a). An apparent lack of unoccupied territories has been noted in many cooperative breeders (e.g. Selander 1964, Ridpath 1972, Woolfenden 1975, Ligon and Ligon 1978, Walters and Walters 1980, Zack and Ligon 1985, Koford et al. 1986), but not all (Rabenold 1985). In species to which the habitat-saturation hypothesis has been applied, helpers remain on their natal territory and compete for breeding vacancies on and in the immediate vicinity of the natal territory (stay-andforay, abbreviated SAF), rather than dispersing after fledging to wander in search of a breeding vacancy (depart-and-search, DAS; Brown 1987). Those practicing SAF appear to have an advantage in competing for positions in their vicinity over those practicing DAS (Zack and Rabenold 1989), perhaps because they can monitor the availability of those positions much more effectively. The demographic conditions under which SAF may be selected over DAS have been mod-

An individual-based, spatially-explicit simulation model of the population dynamics of the endangered red-cockaded woodpecker, Picoides borealis

Spatially-explicit population models allow a link between demography and the landscape. We developed a spatially-explicit simulation model for the red-cockaded woodpecker, Picoides borealis, an endangered and territorial cooperative breeder endemic to the southeastern United States. This kind of model is especially appropriate for this species because it can incorporate the spatial constraints on dispersal of helpers, and because territory locations are predictable. The model combines demographic data from a long-term study with a description of the spatial location of territories. Sensitivity analysis of demographic parameters revealed that population stability was most sensitive to changes in female breeder mortality, mortality of female dispersers and the number of fledglings produced per brood. Population behavior was insensitive to initial stage distribution; reducing the initial number of birds by one-half had a negligible effect. Most importantly, we found that the spatial distribution of territories had as strong an effect on response to demographic stochasticity as territory number. Populations were stable when territories were highly aggregated, with as few as 49 territories. When territories were highly dispersed, more than 169 territories were required to achieve stability. Model results indicate the importance of considering the spatial distribution of territories in management plans, and suggest that this approach is worthy of further development.

INBREEDING DEPRESSION AND ITS EFFECTS ON NATAL DISPERSAL IN RED-COCKADED WOODPECKERS

Abstract Natal dispersal is a key life-history component that may be influenced by the fitness consequences of inbreeding. We studied natal dispersal and inbreeding within a large population of cooperatively breeding, endangered Red-cockaded Woodpeckers (Picoides borealis). We assessed the costs of close inbreeding, the spatial distribution of related males and its relationship to dispersal distance of females, and the change in dispersal behavior of females in the presence of closely related males. Close inbreeding resulted in a significant loss of fitness, through two separate effects: closely related pairs (kinship coefficient ≥ 0.125) exhibited lowered hatching rates and lowered survival and recruitment of fledglings relative to unrelated pairs. Despite a highly predictable spatial clustering of closely related males near the females natal territory, natal dispersal distance of females was not sufficient to avoid these males as mates. Females changed dispersal behavior in the presence of closely related males on the natal territory: female fledglings were significantly more likely to disperse from natal territories if there were closely related males breeding there in the following year. Females did not change dispersal behavior in the presence of related males that were not on the natal territory. We suggest that dispersal behavior is a trade-off between benefits of short-distance dispersal, e.g., an advantage in competing for scarce breeding vacancies, and the substantial cost of close inbreeding.

Evaluating management alternatives for red-cockaded woodpeckers: a modeling approach

Managers often must evaluate an array of enhancement proposals for endangered species. We present a male-only, stage-based matrix model to assess potential effects of various management techniques used to enhance red-cockaded woodpecker (Picoides borealis) populations. We analyzed the elasticity of population growth to changes in each matrix parameter and predicted the population-level effects of 5 proposed management techniques that affect stage-specific survival, growth, and fecundity. Maintaining existing habitat and increasing the number of nesting cavities in unoccupied, but suitable, habitat are most likely to help restore declining populations

Genetic evidence for monogamy in the cooperatively breeding red-cockaded woodpecker

We examined the genetic relationship among putative parents, offspring, and helpers in 224 red-cock-aded woodpeckers (Picoides borealis) from the Sandhills of North Carolina. Comparison of DNA similarity with a pedigree constructed from 3,823 individually-marked birds observed from 1979 to 1992 provided verification of observed relatedness in the sampled population (R2 = 0.87, df = 14, P < 0.001). In this population, breeding pairs may or may not have helpers, most of which are males that remain on their natal territory. Our sample included helpers assisting their parents, helpers assisting a related male and an unrelated female, and helpers assisting an unrelated pair. Band by band comparison and examination of similarity among DNA profiles indicated that all offspring from non-helped nests were sired by their putative parents (n = 28 families). Similarly, all but one offspring in helped nests were also sired by their putative parents (n = 16 families). In the exceptional case, the offspring evidently was sired by a male external to the group. Analysis of similarity values supported the conclusion that matings by helpers or extra-group males are rare or non-existent. Our results indicate that in this species advantages gained by individuals remaining on their natal territories as helpers do not generally include siring offspring.

BETWEEN‐YEAR BREEDING DISPERSAL IN RED‐COCKADED WOODPECKERS: MULTIPLE CAUSES AND ESTIMATED COST

We studied between-year dispersal of adult females within a population of cooperatively breeding Red-cockaded Woodpeckers (Picoides borealis) in the Sandhills of North Carolina, using data collected between 1980 and 1995. We tested four hypotheses about the cause of breeding dispersal: inbreeding avoidance, mate choice, site choice, and social constraints. In addition, we assessed relationships among age, reproductive failure, and breeding dispersal, and we estimated cost of breeding dispersal by plotting mortality against dispersal rate as a function of circumstance. Breeding dispersal in the population that we studied is associated with multiple factors. Inbreeding avoidance influences dispersal of females whose sons inherit their natal terri- tories. Mate choice influences dispersal of females whose mates have died; these females acquire older, higher quality mates by dispersing. In this study, there was no clear rela- tionship between site choice and breeding dispersal. Social constraints do not appear to affect breeding dispersal in this population: no evidence was found to suggest that dispersal is associated with female-female competition, within-group competition for resources, or reproductive competition between mothers and helper sons. The effect of reproductive failure on breeding dispersal changes with female age. Re- productive failure is associated with breeding dispersal in young females only (those <3 yr old). Estimated mortality rates for breeding females that attempt to disperse vs. those that do not attempt to disperse were 59% and 26%, respectively; the difference between those rates is the estimated cost of breeding dispersal in this population, an additional 33% probability of mortality. Thus, breeding females more than double their risk of mortality by dispersing.

SOCIAL AND ENVIRONMENTAL FACTORS AFFECT NATAL DISPERSAL AND PHILOPATRY OF MALE RED‐COCKADED WOODPECKERS

Natal dispersal behavior can vary considerably among individuals, but the causes of intraspecific plasticity in dispersal are poorly understood. We tested six hypotheses about social and environmental conditions that might influence natal dispersal of males in the cooperatively breeding Red-cockaded Woodpecker (Picoides borealis). Further, we examined whether variation in dispersal behavior is heritable. Dispersing from the natal territory during the first year rather than remaining as a helper was associated with four factors. First, dispersing male fledglings were, on average, significantly lower in body mass than their philopatric siblings, indicating an influence of social dominance on dispersal. Second, individuals were more likely to disperse from territories with many male fledglings, independent of the number of adult male helpers per territory, suggesting that sibling (rather than helper–offspring) competition for future reproduction may be the underlying mechanism. Third, the probability of remaining as a helper rather than dispersing was positively associated with quality of the natal territory and with the number of high-quality territories close to the natal site. This suggests an influence of the benefits of philopatry, because many males that initially remain as helpers eventually become breeders on the natal territory or a neighboring territory. Finally, we found evidence that ecological constraints influence dispersal: the probability of dispersing was positively related to the availability of vacant territories in the wider neighborhood of the natal site. Natal dispersal behavior was not influenced by resource competition, measured as group size on the natal territory, or by local density, estimated as the number of active territories in the vicinity of the natal site. Based on comparisons of father–son and brother–brother dispersal behavior, we found no evidence for heritability of philopatric behavior. Dispersal of male fledgling Red-cockaded Woodpeckers can be viewed as conditional on social and ecological factors in the natal territory and in the immediate neighborhood. These factors seem to serve as proximate cues that influence young birds to either disperse or remain as philopatric helpers.

Delayed dispersal and reproduction as a life history tactic in cooperative breeders : fitness calculations from red-cockaded woodpeckers

The evolution of delayed dispersal and reproduction in cooperative breeders can be viewed as selection between alternative life-history tactics: (1) stay-and-foray (SAF), in which individuals delay dispersal and reproduction and compete for breeding vacancies in the vicinity of the natal territory, and (2) depart-and-search (DAS), in which individuals disperse soon after fledging to wander in search of a breeding vacancy. Using demographic data collected from red-cockaded woodpeckers (Picoides borealis), we evaluated a demographic model of the evolution of delayed dispersal and reproduction based on selection between these tactics. Because males of this species exhibit both tactics regularly, we could estimate all model parameters directly. Our estimates provide empirical support for key assumptions of demographic models of the evolution of delayed dispersal and reproduction, such as a disparity in survival between those adopting SAF and those adopting DAS during the first year of life, a low rate of successful dispersal in those practicing DAS, and low reproductive success at early ages among breeders. We show, in a population in which the fate of dispersers could be documented, that the fitness of individuals delaying dispersal and reproduction can equal or exceed that of individuals attempting early reproduction, even without indirect fitness benefits due to helping behavior.

Genetic and Environmental Influences on Natal Dispersal Distance in a Resident Bird Species

We analyzed more than 1,600 dispersal events from two populations of a North American cooperatively breeding woodpecker species to determine what factors influence natal dispersal distance and whether distance traveled affects reproduction later in life. We found significant heritability of natal dispersal distance, in both males and females, indicating substantial additive genetic variance for this behavioral trait. Natal dispersal distance additionally was affected by social and ecological factors: individuals dispersing in their first year of life moved longer distances than those staying on their natal site as helpers for a prolonged time prior to dispersal, and increasing territory isolation led to longer dispersal distances. Successful dispersers incurred fitness costs, with lifetime fledgling production (in both sexes) and lifetime production of recruits to the breeding population (in females only) decreasing with increasing natal dispersal distance. We conclude that natal dispersal distance has a genetic basis but is modulated by environmental and social factors and that natal dispersal distance in this species is (currently) under selection.