Inclusive Fitness May Explain Some but Not All Benefits Derived from Helping Behavior in a Cooperatively Breeding Bird.

AbstractIn cooperative breeding systems, inclusive fitness theory predicts that nonbreeding helpers more closely related to the breeders should be more willing to provide costly alloparental care and thus have more impact on breeder fitness. In the red-cockaded woodpecker (Dryobates borealis), most helpers are the breeders' earlier offspring, but helpers do vary within groups in both relatedness to the breeders (some even being unrelated) and sex, and it can be difficult to parse their separate impacts on breeder fitness. Moreover, most support for inclusive fitness theory has been positive associations between relatedness and behavior rather than actual fitness consequences. We used functional linear models to evaluate the per capita effects of helpers of different relatedness on eight breeder fitness components measured for up to 41 years at three sites. In support of inclusive fitness theory, helpers more related to the breeding pair made greater contributions to six fitness components. However, male helpers made equal contributions to increasing prefledging survival regardless of relatedness. These findings suggest that both inclusive fitness benefits and other direct benefits may underlie helping behaviors in the red-cockaded woodpecker. Our results also demonstrate the application of an underused statistical approach to disentangle a complex ecological phenomenon.

Cavities excavated by woodpeckers limit populations of other cavity-nesting birds.

Research Highlight: Trzcinski, M., Cockle, K., Norris, A., Edworthy, A., Wiebe, K., & Martin, K. (2022). Woodpeckers maintain the diversity of cavity-nesting vertebrates in a temperate forest. Journal of Animal Ecology, https://doi.org/10.1111/1365-2656.13626. Whether populations of hole-nesting birds are limited by the availability of cavities is a long-standing, fundamental question in avian community ecology. The structure of cavity-nesting communities, known as nest webs, includes links between tree species that provide natural holes and bird species that nest in those holes (secondary cavity nesters, SCNs), tree species that provide substrates for cavity excavation and bird species such as woodpeckers that create cavities using those substrates (primary cavity nesters, PCNs), and between PCNs and SCNs. Trzcinski et al. (2022) focus on the latter links and provide the most compelling empirical evidence to date that cavities created by PCNs specifically, as opposed to natural holes or holes generally, limit populations of SCNs. Using data from a long-term study, the authors employ three analyses to separate effects of availability of cavities from environmental factors such as food, habitat features and host tree abundance, while controlling for annual variation and autocorrelation within sites, to isolate the relationship between excavated cavities and SCN numbers. They show that nest density of SCNs is positively related to PCN nest density the previous year, an indicator of availability of excavated cavities, and that the effect of PCNs is stronger when other variables are accounted for. North American coniferous forests such as that studied by Trzcinski et al. (2022) are exceptional in that excavated cavities comprise the vast majority of nesting holes. Whether their findings apply to other systems in which PCNs are a major source of cavities, or to particular PCN-SCN relationships in systems in which excavated cavities account for a much lower proportion of nesting holes remains to be investigated.

Ecosystem-based management for military training, biodiversity, carbon storage and climate resiliency on a complex coastal land/water-scape.

The Defense Coastal/Estuarine Research Program (DCERP) was a 10-year multi-investigator project funded by the Department of Defense to improve understanding of ecosystem processes and their interactions with natural and anthropogenic stressors at the Marine Corps Base Camp Lejeune (MCBCL) located in coastal North Carolina. The project was aimed at facilitating ecosystem-based management (EBM) at the MCBCL and other coastal military installations. Because of its scope, interdisciplinary character, and duration, DCERP embodied many of the opportunities and challenges associated with EBM, including the need for explicit goals, system models, long-term perspectives, systems complexity, change inevitability, consideration of humans as ecosystem components, and program adaptability and accountability. We describe key elements of this program, its contributions to coastal EBM, and its relevance as an exemplar of EBM.

Experimental evidence of a symbiosis between red-cockaded woodpeckers and fungi.

Primary cavity excavators, such as woodpeckers, are ecosystem engineers in many systems. Associations between cavity excavators and fungi have long been hypothesized to facilitate cavity excavation, but these relationships have not been experimentally verified. Fungi may help excavators by softening wood, while excavators may facilitate fungal dispersal. Here we demonstrate that excavators facilitate fungal dispersal and thus we report the first experimental evidence of a symbiosis between fungi and a cavity excavator, the red-cockaded woodpecker (RCW,Picoides borealis). Swab samples of birds showed that RCWs carry fungal communities similar to those found in their completed excavations. A 26-month field experiment using human-made aseptically drilled excavations in live trees, half of which were inaccessible to RCWs, demonstrated that RCWs directly alter fungal colonization and community composition. Experimental excavations that were accessible to RCWs contained fungal communities similar to natural RCW excavations, whereas inaccessible experimental excavations contained significantly different fungal communities. Our work demonstrates a complex symbiosis between cavity excavators and communities of fungi, with implications for forest ecology, wildlife management, and conservation.

Population models for social species: lessons learned from models of Red­cockaded Woodpeckers (Picoides borealis).

Behavior can have major impacts on the population dynamics of social species and should be incorporated into demographic models to realistically evaluate population trends and extinction risk. We compared the predictions of a stage- and age-based matrix model, an individual-based model (IBM, developed in the program Vortex), and a spatially explicit individual-based model (SEPM) with the actual dynamics of a population of Red-cockaded Woodpeckers (RCW; Picoides borealis) in the Sandhills of North Carolina, USA. Predictions, including population size, composition, and growth rate, differed the most from actual population characteristics for models that did not incorporate social structure. The SEPM most closely predicted actual population dynamics, underestimating the population by 2.3%. This model, specifically developed to simulate RCW population dynamics, contains many of the features that we assert are important for adequately incorporating social behavior into demographic and population modeling. These features include the ability to (1) differentiate individuals based on their stage class, (2) capture the dynamics of the population at both the individual and group level, (3) incorporate the positive or negative effects of subdominants, (4) include environmental and demographic stochasticity, and (5) capture dispersal and other spatial factors. The RCW SEPM, although currently species-specific, provides a strong blueprint for how population models for social species could be constructed in the future when data allow.

Defining and evaluating the umbrella species concept for conserving and restoring landscape connectivity.

Conserving or restoring landscape connectivity between patches of breeding habitat is a common strategy to protect threatened species from habitat fragmentation. By managing connectivity for some species, usually charismatic vertebrates, it is often assumed that these species will serve as conservation umbrellas for other species. We tested this assumption by developing a quantitative method to measure overlap in dispersal habitat of 3 threatened species-a bird (the umbrella), a butterfly, and a frog-inhabiting the same fragmented landscape. Dispersal habitat was determined with Circuitscape, which was parameterized with movement data collected for each species. Despite differences in natural history and breeding habitat, we found substantial overlap in the spatial distributions of areas important for dispersal of this suite of taxa. However, the intuitive umbrella species (the bird) did not have the highest overlap with other species in terms of the areas that supported connectivity. Nevertheless, we contend that when there are no irreconcilable differences between the dispersal habitats of species that cohabitate on the landscape, managing for umbrella species can help conserve or restore connectivity simultaneously for multiple threatened species with different habitat requirements.

Experimental support for food limitation of a short-distance migratory bird wintering in the temperate zone.

The Winter Food Limitation Hypothesis (WFLH) states that winter food abundance is a dominant source of population limitation of migratory birds. Evidence is accumulating that long-distance migratory birds wintering in tropical climates have high overwinter survival probabilities and that winter food limitation mainly affects their fitness nonlethally by limiting energetic reserves necessary for successful reproduction. In contrast, the relative roles of direct mortality vs. indirect effects caused by food limitation have not been investigated thoroughly on short-distance migratory birds wintering in temperate zones, where they face thermal challenges. We performed the first test of the WFLH for a temperate migratory bird in the wild on the Swamp Sparrow (Melospiza georgiana), with a replicated plot-wide food supplementation experiment. In contrast to tropical, but consistent with other temperate-wintering migrants, Swamp Sparrows on unmanipulated plots showed relatively low apparent survival across the winter. Following food addition, birds (1) immigrated to experimental plots, which subsequently supported approximately 50% higher abundances, (2) experienced increases of within-season apparent survival of 8-10%, depending on age/sex class, and (3) had higher-scaled mass index values, all supporting winter food limitation. The last two findings are interrelated because birds with higher scaled mass had higher survival probabilities, further supporting direct effects of winter food limitation. Food limitation of fat reserves might also have indirect effects on reproductive success by limiting migration timing and survival during migration. Increases in scaled mass were higher in females, suggesting that they are disproportionately affected by food limitation, possibly through competition. Based on Robust Design Modeling, we found no support for emigration prior to food addition, indicating that our estimates of mortality are unbiased.

Variation in migratory behavior influences regional genetic diversity and structure among American Kestrel populations (Falco sparverius) in North America.

Birds employ numerous strategies to cope with seasonal fluctuations in high-quality habitat availability. Long distance migration is a common tactic; however, partial migration is especially common among broadly distributed species. Under partial migration systems, a portion of a species migrates, whereas the remainder inhabits breeding grounds year round. In this study, we identified effects of migratory behavior variation on genetic structure and diversity of American Kestrels (Falco sparverius), a widespread partial migrant in North America. American Kestrels generally migrate; however, a resident group inhabits the southeastern United States year round. The southeastern group is designated as a separate subspecies (F. s. paulus) from the migratory group (F. s. sparverius). Using mitochondrial DNA and microsatellites from 183 and 211 individuals, respectively, we illustrate that genetic structure is stronger among nonmigratory populations, with differentiation measures ranging from 0.060 to 0.189 depending on genetic marker and analysis approach. In contrast, measures from western North American populations ranged from 0 to 0.032. These findings suggest that seasonal migratory behavior is also associated with natal and breeding dispersal tendencies. We likewise detected significantly lower genetic diversity within nonmigratory populations, reflecting the greater influence of genetic drift in small populations. We identified the signal of population expansion among nonmigratory populations, consistent with the recent establishment of higher latitude breeding locations following Pleistocene glacial retreat. Differentiation of F. s. paulus and F. s. sparverius reflected subtle differences in allele frequencies. Because migratory behavior can evolve quickly, our analyses suggest recent origins of migratory American Kestrel populations in North America.

Effects of cavity orientation on nesting success inferred from long-term monitoring of the endangered red-cockaded woodpecker.

Animals that create structures often display non-random patterns in the direction of their constructions. This tendency of oriented construction is widely presumed to be an adaptive trait of the constructor's extended phenotype, but there is little empirical support for this hypothesis. Particularly, for cavity nesting-birds there is a lack of studies examining this issue. In this study of a primary cavity excavator, the endangered red-cockaded woodpecker (Dryobates borealis), we show that cavity entrances exhibited a strong westward bias in all 11 of the populations examined throughout the geographic range of the species in the southeastern United States. This species requires cavities in living pine trees for roosting and nesting that often take many years to complete, resulting in many incomplete excavations on the landscape. We used population monitoring data to show that orientation was stronger among completed cavities than incomplete cavities. There was a significant correlation between latitude and average cavity direction among populations, turning northward with increasing latitude, suggesting adaptation to local conditions. Long-term monitoring data showed that cavity orientation and breeding group size are correlated with egg hatching rates, fledging rates, and the total number of fledglings produced per nest. Our results provide empirical evidence from extensive long-term data that directional orientation in animal constructions is an important feature of the extended animal phenotype and have immediate implications for animal ecology and the conservation of endangered species.

Changes in genetic diversity and differentiation in Red-cockaded woodpeckers (Dryobates borealis) over the past century.

Red-cockaded woodpeckers (RCW; Dryobates borealis) declined after human activities reduced their fire-maintained pine ecosystem to <3% of its historical range in the southeastern United States and degraded remaining habitat. An estimated 1.6 million RCW cooperative breeding groups declined to about 3,500 groups with no more than 10,000 birds by 1978. Management has increased RCW population abundances since they were at their lowest in the 1990s. However, no range-wide study has been undertaken since then to investigate the impacts of this massive bottleneck or infer the effects of conservation management and recent demographic recoveries. We used mitochondrial DNA sequences (mtDNA) and nine nuclear microsatellite loci to determine if range-wide demographic declines resulted in changes to genetic structure and diversity in RCW by comparing samples collected before 1970 (mtDNA data only), between 1992 and 1995 (mtDNA and microsatellites), and between 2010 and 2014 (mtDNA and microsatellites). We show that genetic diversity has been lost as detected by a reduction in the number of mitochondrial haplotypes. This reduction was apparent in comparisons of pre-1970 mtDNA data with data from the 1992-1995 and 2010-2014 time points, with no change between the latter two time points in mtDNA and microsatellite analyses. The mtDNA data also revealed increases in range-wide genetic differentiation, with a genetically panmictic population present throughout the southeastern United States in the pre-1970s data and subsequent development of genetic structure that has remained unchanged since the 1990s. Genetic structure was also uncovered with the microsatellite data, which like the mtDNA data showed little change between the 1992-1995 and 2010-2014 data sets. Temporal haplotype networks revealed a consistent, star-like phylogeny, suggesting that despite the overall loss of haplotypes, no phylogenetically distinct mtDNA lineages were lost when the population declined. Our results may suggest that management during the last two decades has prevented additional losses of genetic diversity.

Cavity excavation and enlargement as mechanisms for indirect interactions in an avian community.

Direct and indirect species interactions within ecological communities may play a strong role in influencing or maintaining community structure. Complex community interactions pose a major challenge to predicting ecosystem responses to environmental change because predictive frameworks require identification of mechanisms by which community interactions arise. Cavity-nesting communities are well suited for mechanistic studies of species interactions because cavity nesters interact through the creation of and competition for cavity-nest sites. In this study, we use a cavity-nest web as a predictive framework for identifying potential indirect species interactions within a cavity-nesting community. From 2002 to 2005, we monitored abundance and nests of cavity-nesting birds in the longleaf pine (Pinus palustris) ecosystem. Using a nest-web approach, we identified a potential indirect interaction between the Red-cockaded Woodpecker (Picoides borealis) and large secondary cavity nesters, mediated by the Northern Flicker (Colaptes auratus). We used structural equation modeling to test a path model of this interaction, using cavity excavation and enlargement as mechanisms which drive the relationship between these species. Through experimental manipulation of cavity availability, we blocked links described in our model, confirming cavity creation and enlargement as processes that influence community structure. We found that a single-species management technique could potentially disrupt this indirect relationship by affecting Northern Flicker cavity-excavation behavior. This study is the first demonstration of how experimental cavity manipulation can be used to test inferred processes derived from a nest web and highlights the need to understand how mechanisms underlying species interactions can complicate ecosystem responses to environmental change.

Can we improve estimates of juvenile dispersal distance and survival?

Estimates of distributions of natal dispersal distances and juvenile recruitment rates in open populations are strongly influenced by the extent and shape of the areas sampled. Techniques to improve biased dispersal and survival estimates include area-ratio methods based on weighting observations by sampling effort, the extent and shape of the area sampled, and the amount and distribution of preferred habitat surrounding the area sampled. We partitioned territories within the boundaries of a large, almost geographically closed, population of individually marked Red-cockaded Woodpeckers (Picoides borealis) and estimated dispersal and survival parameters from hypothetical smaller study areas (sampling areas) of varying sizes and shapes in order to examine whether an area-ratio method provides accurate or improved estimates of juvenile dispersal distance and survival. Non-aggregated sampling areas resulted in the detection of fewer dispersal events, but because of their large spatial extent, produced unbiased dispersal estimates. The use of aggregated sampling areas (circular or linear) resulted in the detection of higher numbers of dispersal events, but produced biased dispersal estimates that were generally improved by the area-ratio method. Area-ratio corrections usually provided better estimates of median dispersal distance than uncorrected estimates. Survival to breeding was usually underestimated and often not improved by the area-ratio method, regardless of extent and shape of the sampling area. Estimates of juvenile survival to breeding were improved by assuming that rates of emigration were equivalent to immigration, and correcting survival estimates accordingly. Small, local studies should use an area-ratio method to improve their estimates of median dispersal distance. Because the correction method estimates relative, but not absolute, numbers of individuals dispersing across distance categories, the area-ratio method should not be used for estimating survival. Non-aggregated sampling areas may be an effective design to increase spatial extent (and thus decrease bias) without proportionately increasing the amount of habitat sampled.

Body Condition Indices Predict Reproductive Success but Not Survival in a Sedentary, Tropical Bird.

Body condition may predict individual fitness because those in better condition have more resources to allocate towards improving their fitness. However, the hypothesis that condition indices are meaningful proxies for fitness has been questioned. Here, we ask if intraspecific variation in condition indices predicts annual reproductive success and survival. We monitored a population of Neochmia phaeton (crimson finch), a sedentary, tropical passerine, for reproductive success and survival over four breeding seasons, and sampled them for commonly used condition indices: mass adjusted for body size, muscle and fat scores, packed cell volume, hemoglobin concentration, total plasma protein, and heterophil to lymphocyte ratio. Our study population is well suited for this research because individuals forage in common areas and do not hold territories such that variation in condition between individuals is not confounded by differences in habitat quality. Furthermore, we controlled for factors that are known to impact condition indices in our study population (e.g., breeding stage) such that we assessed individual condition relative to others in the same context. Condition indices that reflect energy reserves predicted both the probability of an individual fledging young and the number of young produced that survived to independence, but only during some years. Those that were relatively heavy for their body size produced about three times more independent young compared to light individuals. That energy reserves are a meaningful predictor of reproductive success in a sedentary passerine supports the idea that energy reserves are at least sometimes predictors of fitness. However, hematological indices failed to predict reproductive success and none of the indices predicted survival. Therefore, some but not all condition indices may be informative, but because we found that most indices did not predict any component of fitness, we question the ubiquitous interpretation of condition indices as surrogates for individual quality and fitness.

Sex-Ratio Selection in Species with Helpers at the Nest: The Repayment Model Revisited.

We reexamine the theoretical and empirical basis for the "repayment model" of Emlen, Emlen, and Levin, which predicts that the overall sex ratio of offspring in cooperative-breeding species with helpers at the nest should be biased toward the more helpful sex. We conclude that in theory the model may yield a biased sex ratio but only under restricted conditions that are unlikely to be met in most populations. In those cases where the model is potentially applicable, estimates of both direct and indirect fitness of sons and daughters are necessary in order to avoid double accounting. As a result, extensive demographic data are required to determine the expected sex-ratio bias. Empirically, none of the three examples originally suggested as supporting the repayment model withstand critical scrutiny. Using long-term demographic data from two populations of one of these species, the red-cockaded woodpecker (Picoides borealis), we determine that the model predicts a biased sex ratio not observed in the data. This suggests that confounding factors may counter the sex-ratio bias predicted by the model, that the extensive empirical data available for this species may be insufficient to test the model, or that there are as yet unknown theoretical difficulties with the model. Finally, we discuss the recently reported case of the Seychelles warbler (Acrocephalus sechellensis). The extraordinarily biased sex ratios reported in this species are in accord with those predicted by the model when applied at the scale of individual groups but not at the population level. Additional empirical work is necessary to determine what, if any, the generality and usefulness of the repayment model may be.

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.

Inbreeding and experience affect response to climate change by endangered woodpeckers.

In recent decades, female red-cockaded woodpeckers (Picoides borealis) have laid eggs increasingly earlier in response to a changing climate, as has been observed in several other bird species breeding at north temperate latitudes. Within each year, females that lay earlier are more productive than females that lay later. However, inexperienced females, experienced females who change mates and inbred birds have not adjusted to the changing climate by laying earlier, and have suffered reproductive costs as a result. Failure to respond to global climate change may be a further example of the reduced ability of inbred animals to respond to environmental challenges.

Variation in body condition indices of crimson finches by sex, breeding stage, age, time of day, and year.

Body condition indices are increasingly applied in conservation to assess habitat quality, identify stressed populations before they decline, determine effects of disturbances, and understand mechanisms of declines. To employ condition indices in this manner, we need first to understand their baseline variability and sources of variation. Here, we used crimson finches (Neochmia phaeton), a tropical passerine, to describe the variation in seven commonly used condition indices by sex, age, breeding stage, time of day, and year. We found that packed cell volume, haemoglobin, total plasma protein, and scaled mass were all significantly affected by an interaction between sex and breeding stage. Furcular fat varied by sex and breeding stage and also trended by year, scaled mass showed a positive trend with age and varied by time of day, and haemoglobin additionally varied by year. Pectoral muscle scores varied and heterophil to lymphocyte ratio trended only by year. Year effects might reflect a response to annual variation in environmental conditions; therefore, those indices showing year effects may be especially worthy of further investigation of their potential for conservation applications. Pectoral muscle scores and heterophil to lymphocyte ratio may be particularly useful due to the lack of influence of other variables on them. For the other indices, the large variation that can be attributed to individual covariates, such as sex and breeding stage, suggests that one should not interpret the physiological condition of an individual as measured by these indices from their absolute value. Instead, the condition of an individual should be interpreted relative to conspecifics by sex, breeding stage, and possibly age.

Proximate and ultimate factors that promote aggregated breeding in the Western Sandpiper.

We report that Western Sandpipers (Calidris mauri) on Alaska's Yukon-Kuskokwim River Delta exhibited aggregated breeding behavior at a relatively small spatial scale. Prior to clutch initiation, males performing song flight displays on a 36 ha plot were aggregated as were subsequent initial nesting attempts on the plot. We tested three hypotheses commonly invoked to explain aggregated breeding in territorial species (social mate choice, predation, and material resources hypotheses), and found support for the material resources hypothesis, as dispersed individuals were more often associated with tundra habitat patches, and aggregated individuals nested more often in undulating-tundra habitat patches compared to patch availability. The pattern of habitat occupancy conformed to an ideal despotic distribution with aggregated nesting birds in undulating-tundra patches experiencing lower reproductive success. On our study plot, older, more aggressive males solicited females more often, and defended larger, more dispersed sites in tundra habitat patches, compared to younger, less aggressive males that were aggregated in undulating-tundra habitat patches. Breeding aggregations are often concentrated on or near a critical resource. In contrast, Western Sandpiper breeding aggregations occur when dominant and/or older individuals exclude younger, subordinate individuals from preferred habitat. Although many taxa of non-colonial birds have been reported to aggregate breeding territories, this is the first quantitative report of aggregated breeding behavior in a non-colonial monogamous shorebird species prior to hatch.

Causes of reduced clutch size in a tidal marsh endemic.

We tested three hypotheses of clutch size variation in two subspecies of the swamp sparrow (Melospiza georgiana georgiana and M. g. nigrescens). Swamp sparrows follow the pattern of other estuarine endemics, where clutch size is smaller among tidal salt marsh populations (M. g. nigrescens) than their closest inland relatives (M. g. georgiana). Our results support predation risk and temperature, but not adult survival, as explanations of this pattern in swamp sparrows. Coastal nests were twice as likely to fail as inland nests, and parental activity around the nest site was positively related to clutch size at both sites. When brood size was controlled for, coastal adults visited nests less often and females vocalized less frequently during visits than inland birds, which may decrease nest detectability to predators. Coastal parents waited longer than inland birds to feed offspring in the presence of a model nest predator, but there was no difference in their response to models of predators of adults, as would be expected if coastal birds possessed increased longevity. Additionally, coastal females laid more eggs than inland females over a single season, following a within-season bet-hedging strategy rather than reducing within-season investment. Coastal territories experienced ambient air temperatures above the physiological zero of egg development more often, and higher temperatures during laying correlated with smaller clutches and increased egg inviability among coastal birds. Similar effects were not seen among inland nests, where laying temperatures were generally below physiological zero. Both subspecies showed an increase in hatching asynchrony and a decrease in apparent incubation length under high temperatures. Coastal individuals, however, showed less hatching asynchrony overall despite higher temperatures. Both air temperatures during laying and predation risk could potentially explain reduced clutch size in not only coastal plain swamp sparrows, but also other tidal marsh endemics.