Reed Bowman

Avian ecology and conservation in an urbanizing world

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A historical perspective on urban bird research: trends, terms, and approaches

As Earth’s human population continues to increase and urbanize, it is likely to increasingly affect biodiversity. Avian ecologists have been studying these effects for over a century. Here, we review these studies to: 1) characterize the type of research approaches that have been used, 2) suggest strengths and weaknesses of these approaches, 3) offer a standardized nomenclature for the degree of settlement that will be used throughout this volume, and 4) suggest how our approach can be strengthened to better inform public policy. The majority of urban bird studies were conducted since 1980. The typical study is a one- or two-year correlational investigation of breeding bird relative abundance in the forests of the United States or northern Europe. Experimental studies are rare despite the frequent and replicated land transformations conducted by developers. Studies of birds in tropical, urban settings are especially rare. This is problematic because human populations are expected to rapidly grow and urbanize in such regions and biodiversity there is rich. Recognizing trade-offs among study duration, spatial extent, and mechanistic understanding, we suggest that researchers use short-term, correlational studies of the entire gradient of urbanization to inform long-term, mechanistic studies of bird populations. We define five points along the gradient of urbanization for consistent use throughout this volume (wildland, exurban or rural, suburban, and urban;(Table 1.1). These are useful for categorizing study areas at the landscape scale (>km2). Briefly, wildlands are unsettled lands that may occasionally include dwellings. Rural and exurban lands are sparsely settled by individual homesteads, recreational development, and small towns (they are distinguished by the surrounding matrix: rural = agricultural, exurban = native habitat). Suburban lands are characterized by moderate- to high-density, single-family housing with lot sizes of 0.1-1.0 ha. Urban lands are primarily covered by multi-family and/or multi-storied buildings. Urban bird studies would more effectively inform policy, planning, and management if they were more relevant, rigorous, compelling, and visible. We suggest that this can be accomplished by 1) understanding how development pattern affects birds, 2) increasing study of birds in tropical urban areas, 3) increasing the use of experimental, mechanistic investigations, 4) using landscape ecological metrics to quantify the urban settings we study, and 5) distilling clear graphs or photographs of important results.

Congruent population structure inferred from dispersal behaviour and intensive genetic surveys of the threatened Florida scrub‐jay (Aphelocoma cœrulescens)

The delimitation of populations, defined as groups of individuals linked by gene flow, is possible by the analysis of genetic markers and also by spatial models based on dispersal probabilities across a landscape. We combined these two complimentary methods to define the spatial pattern of genetic structure among remaining populations of the threatened Florida scrub‐jay, a species for which dispersal ability is unusually well‐characterized. The range‐wide population was intensively censused in the 1990s, and a metapopulation model defined population boundaries based on predicted dispersal‐mediated demographic connectivity. We subjected genotypes from more than 1000 individual jays screened at 20 microsatellite loci to two Bayesian clustering methods. We describe a consensus method for identifying common features across many replicated clustering runs. Ten genetically differentiated groups exist across the present‐day range of the Florida scrub‐jay. These groups are largely consistent with the dispersal‐defined metapopulations, which assume very limited dispersal ability. Some genetic groups comprise more than one metapopulation, likely because these genetically similar metapopulations were sundered only recently by habitat alteration. The combined reconstructions of population structure based on genetics and dispersal‐mediated demographic connectivity provide a robust depiction of the current genetic and demographic organization of this species, reflecting past and present levels of dispersal among occupied habitat patches. The differentiation of populations into 10 genetic groups adds urgency to management efforts aimed at preserving what remains of genetic variation in this dwindling species, by maintaining viable populations of all genetically differentiated and geographically isolated populations.

Food supplementation and possible mechanisms underlying early breeding in the Florida Scrub-Jay (Aphelocoma coerulescens).

Food supplementation studies demonstrate the importance of resources in the timing of reproduction. Studies of Florida Scrub-Jays (Aphelocoma coerulescens) found that supplemented jays bred earlier than unsupplemented jays and that protein may play a critical role. In this study, free-living scrub-jays were provided with supplemental diets high in fat and protein (HFHP) or high in fat and low in protein (HFLP). Jays in both treatments bred earlier than unsupplemented controls (CNT), but HFHP-supplemented jays bred earlier than HFLP jays. To assess possible mechanisms, we measured testosterone (T) in males, estradiol (E2) in females, and corticosterone (CORT) in both. HFHP males had higher T than HFLP and CNT males, but treatment did not affect E2 levels of females. Pilot studies of scrub-jays in suburban environments suggest that the spatial and temporal predictability of food may influence corticosterone (CORT) levels. Suburban jays have year-round access to human-provided foods and breed earlier than wildland jays; thus, we compared CORT in all treatments in the natural site (wildlands) with those of suburban jays. CORT levels of suburban jays were lower than HFLP, HFHP, and CNT jays. HFHP-supplemented jays had lower CORT levels than those of HFLP and CNT jays. The observed differences in the timing of breeding, both between suburban and wildland populations and between experimental groups in the wildlands, may result from differences in the spatial and temporal predictability of food, and the nutritional differences in diets. Because CORT can negatively affect the reproductive axis, we postulate that nutrient availability, the predictability of food, CORT levels, and initiation of reproduction are inextricably linked.

Nutritional quality of prebreeding diet influences breeding performance of the Florida scrub-jay

Food supplementation studies of breeding birds have traditionally concentrated on energetic constraints on breeding performance. It is only recently that the nutritional quality of the prebreeding diet has also been considered influential. We examined the importance of specific nutrients in the prebreeding diet of the Florida scrub-jay (Aphelocoma coerulescens). Birds were provided with one of two supplements (rich in protein and fat or rich in fat only) prior to breeding in 2000 and 2001 and their breeding performance, in relation to unsupplemented (control) birds, was examined. Birds receiving both supplements significantly advanced laying in both years, and increased clutch size in 2000 but not in 2001. Laying date explained variation in clutch size in birds on dietary supplements. Egg mass and volume declined with laying order, irrespective of dietary treatment, but birds on the high fat, high protein diet laid heavier third eggs than controls and this was independent of laying date. Laboratory analysis of 14 abandoned and unhatched eggs revealed that as egg mass increased so did the absolute amount of protein and water while fat content remained relatively fixed. Using these relationships between the masses of egg components and fresh egg mass, we calculated that heavier third eggs laid by birds on high fat and high protein, compared with those laid by controls, contained more water that may be fundamental to chick growth and survival. This is the first demonstration for an avian species that nutritional quality of prebreeding diet can simultaneously influence laying date, clutch size, and egg size and composition.

Does Differential Access to Protein Influence Differences in Timing of Breeding of Florida Scrub-Jays (Aphelocoma coerulescens) in Suburban and Wildland Habitats?

Abstract Timing of breeding in Florida Scrub-Jays (Aphelocoma coerulescens) varies both within and between years. Social status and breeding experience may explain much of the within-year variation, but the availability of certain foods may partially explain between-year patterns. Scrub-jays in suburban habitats with access to unlimited human-provided foods breed earlier and with less between-year variation in timing of breeding than jays in wildland habitats. We hypothesized that those differences in timing of breeding result from access to human-provided foods in the suburban site. Human-provided food may influence timing of breeding by improving the overall body condition of females, or it may influence breeding by providing nutrients essential for breeding. If condition mediated, breeding females in the two habitats should differ in certain physiological parameters relative to time before egg laying and calendar date. If the effect is not related to body condition, we expect differences in prebreeding females relative to calendar date, but not in relation to time before egg laying. To test those predictions, we measured plasma levels of total protein, calcium, luteinizing hormone, and estradiol. We also measured variables associated with body condition—body mass, a size-corrected condition index, and total body lipids. Most variables tended to increase with both days before laying and calendar date, except total body lipids, which decreased. Suburban females had higher levels of plasma protein relative to both days before egg laying and calendar date than female breeders in the wildland habitat. Luteinizing hormone differed between sites relative to calendar date but not days before laying. Our data suggest that suburban scrub-jays with access to predictable sources of high-quality human-provided foods accumulate endogenous protein that can be used to breed earlier.

VARIATION IN FORAGING BEHAVIOR, DIET, AND TIME OF BREEDING OF FLORIDA SCRUB-JAYS IN SUBURBAN AND WILDLAND HABITATS

Abstract Supplemental food enables some birds to lay eggs earlier, perhaps by allowing birds to increase their energy intake or allocate energy from other activities to reproduction. We examined the relationships between prelaying behavior, food handling and consumption rates, and the timing of breeding of female Florida Scrub-Jays (Aphelocoma coerulescens) in suburban and wildland habitats. Scrub-jays in suburban habitats had access to ad libitum human-provided foods; wildland jays did not. During both years of this study, suburban scrub-jays bred earlier than their wildland counterparts. Wildland scrub-jays bred earlier in 1997 than in 1996, but the timing of breeding by suburban scrub-jays did not vary between years. Suburban scrub-jays spent less time foraging and more time perching than wildland jays. They handled more food per hour and per foraging hour, suggesting their foraging was more efficient. Despite this, food consumption rates did not differ between the two habitats. Neither time spent foraging or perching nor food consumption rates significantly influenced variation in time of breeding among individuals. Time of breeding was significantly influenced by site, year, and rate of food handling. Individuals that handled more food items per foraging hour, that is, those individuals that were most efficient, were the earliest breeders in both habitats. These results suggest that foraging efficiency increases with access to human-provided food and that resource predictability may be a perceptual cue for the appropriate timing of breeding. Variación en el Comportamiento de Forrajeo, la Dieta y la Época de Reproducción de Aphelocoma coerulescens en Ambientes Suburbanos y Silvestres Resumen. El alimento suplementario le permite a algunas aves poner huevos más temprano, quizás aumentando su ingestión de energía o permitiendo cambiar la asignación de energía de otras actividades a la reproducción. En este estudio examinamos las relaciones entre el comportamiento pre-postura, la manipulación de alimento y la tasa de consumo con la época de reproducción de hembras de la especie Aphelocoma coerulescens en ambientes suburbanos y silvestres. Las aves en ambientes suburbanos tenían acceso a alimento provisto ad libitum por humanos, mientras que las aves de las áreas silvestres no. Durante los dos años de estudio, las aves suburbanas se reprodujeron más temprano que las de las áreas silvestres. Las aves de áreas silvestres se reprodujeron más temprano en 1997 que en 1996, pero la época reproductiva de las aves de áreas suburbanas no varió entre años. Las aves suburbanas pasaron menos tiempo forrajeando y más tiempo perchadas que las de áreas silvestres, y además manipularon más alimento por hora y por hora de forrajeo, lo que sugiere que forrajearon más eficientemente. Sin embargo, las tasas de consumo de alimento no difirieron entre los dos ambientes. La variación entre individuos en el momento de la reproducción no fue influenciada significativamente por el tiempo invertido en forrajeo o descanso ni por la tasa de consumo de alimento, pero sí por el sitio, el año y la tasa de manipulación de alimento. Los individuos que manipularon más ítems alimenticios por sesión de forrajeo (los más eficientes), fueron los que se reprodujeron más temprano en ambos ambientes. Estos resultados sugieren que la eficiencia de forrajeo aumenta con el acceso a alimentos provistos por humanos y que la predecibilidad de los recursos podría ser percibida como una señal indicadora del momento de reproducción adecuado.

Effects of habitat fragmentation on effective dispersal of Florida scrub-jays.

Studies comparing dispersal in fragmented versus unfragmented landscapes show that habitat fragmentation alters the dispersal behavior of many species. We used two complementary approaches to explore Florida Scrub-Jay (Aphelocoma coerulescens) dispersal in relation to landscape fragmentation. First, we compared dispersal distances of color-marked individuals in intensively monitored continuous and fragmented landscapes. Second, we estimated effective dispersal relative to the degree of fragmentation (as inferred from two landscape indexes: proportion of study site covered with Florida Scrub-Jay habitat and mean distance to nearest habitat patch within each study site) by comparing genetic isolation-by-distance regressions among 13 study sites having a range of landscape structures. Among color-banded individuals, dispersal distances were greater in fragmented versus continuous landscapes, a result consistent with other studies. Nevertheless, genetic analyses revealed that effective dispersal decreases as the proportion of habitat in the landscape decreases. These results suggest that although individual Florida Scrub-Jays may disperse farther as fragmentation increases, those that do so are less successful as breeders than those that disperse short distances. Our study highlights the importance of combining observational data with genetic inferences when evaluating the complex biological and life-history implications of dispersal.

Nest success and the timing of nest failure of Florida Scrub-Jays in suburban and wildland habitats

Urbanization has broad and complex effects on ecological systems. Many of these effects are likely to influence nest success of birds, some positively and others negatively, thus complex interactions among effects are likely to exist that influence patterns of success. Nest success of Florida Scrub-Jays did not differ between a suburban and wildland population or across a human density gradient within the suburban population. Nesting success between egg and nestling stages did not differ in the wildland population, but nest success during the egg stage was high and success during the nestling stage low in the suburban population. As a consequence, nest contents survived longer during the nesting cycle in the suburban population than in the wildland population, even though overall rates of nest success did not differ. In the suburbs, nests with eggs were less likely to be deserted and nests with nestlings were more likely to be depredated or more likely for the nestling to starve than in the wildlands. In both habitats, nest success declined throughout the nesting season. Because suburban birds begin nesting earlier than wildland birds, nests are at a more advanced stage when nest failure rates increase. However, temporal differences in nesting are absent for second and third nest attempts, yet suburban nests still fail later in the nesting cycle. This suggests that site-specific differences exist in the predator community or the behavior of birds increasing their vulnerability to predators that affects timing of nest failure.

Diet quality during pre-laying and nestling periods influences growth and survival of Florida scrub-jay ( Aphelocoma coerulescens ) chicks

Food availability is one of the most important determinants of successful reproduction in birds. In a previous study, it was shown that Florida scrub-jays Aphelocoma coerulescens maintained a third egg mass when supplemented with a high fat and high protein diet during pre-breeding, as opposed to birds that were not supplemented that laid third eggs markedly lighter in mass than first- and second-laid eggs. Increases in egg quality promote chick growth and survival in many avian species. In this study, scrub-jays were provided with supplements throughout the pre-laying and nestling periods of 2001 and 2002 to investigate whether diet quality influenced growth and survival of chicks. Fledging success and survival to independence of unsupplemented chicks were higher for 2002 compared with 2001 indicating that breeding conditions (e.g. natural food availability) for jays were probably improved in the former year. Consistent growth patterns were found during the first 11 days post-hatch between chicks on supplemented and those on unsupplemented territories. Of the three growth measures, only seventh primary feather growth tended to be greater for third-hatched chicks on supplemented territories compared with third-hatched chicks on control territories. Food supplementation influenced survival of chicks. Compared with chicks hatching on unsupplemented territories, fledging success of chicks hatching from second-laid eggs was significantly greater in 2001, but not in 2002. Chicks from third-laid eggs on supplemented territories also tended to survive better in 2001 compared with chicks from unsupplemented territories, but, again, no such effect was found in 2002. We conclude that food supplementation in the pre-laying and nestling periods results in little measurable improvement in chick growth. However, improvements were found in survival of chicks that may be mediated through improvements in egg quality, but also may be the result of changes in foraging strategies of provisioning birds on supplemented territories. Chicks on supplemented territories might be in better body condition than those on unsupplemented ones. Methods other than morphometrics may be required to detect elevations in body condition of chicks raised on supplemented territories.