Low-coverage whole genome sequencing for highly accurate population assignment: Mapping migratory connectivity in the American Redstart (Setophaga ruticilla).

Understanding the geographic linkages among populations across the annual cycle is an essential component for understanding the ecology and evolution of migratory species and for facilitating their effective conservation. While genetic markers have been widely applied to describe migratory connections, the rapid development of new sequencing methods, such as low-coverage whole genome sequencing (lcWGS), provides new opportunities for improved estimates of migratory connectivity. Here, we use lcWGS to identify fine-scale population structure in a widespread songbird, the American Redstart (Setophaga ruticilla), and accurately assign individuals to genetically distinct breeding populations. Assignment of individuals from the nonbreeding range reveals population-specific patterns of varying migratory connectivity. By combining migratory connectivity results with demographic analysis of population abundance and trends, we consider full annual cycle conservation strategies for preserving numbers of individuals and genetic diversity. Notably, we highlight the importance of the Northern Temperate-Greater Antilles migratory population as containing the largest proportion of individuals in the species. Finally, we highlight valuable considerations for other population assignment studies aimed at using lcWGS. Our results have broad implications for improving our understanding of the ecology and evolution of migratory species through conservation genomics approaches.

Behavioral niche partitioning reexamined: Do behavioral differences predict dietary differences in warblers?

Behavioral niche partitioning is an important and widely assumed mechanism for the coexistence of ecologically similar species. Here we assessed this mechanism by testing its core assumption, that evolved differences in foraging behavior correspond with differences in resources consumed. We combined data on foraging behavior, available prey, and observed diets of five coexisting species of New World wood warblers (Parulidae), a system that has been foundational to our understanding of behavioral niche partitioning. Consistent with past work, we found that the five species differed markedly in their foraging behavior, enough that some species pairs hardly overlapped at all in foraging microhabitat. In contrast, the birds overlapped highly in diet, while exhibiting small, interpretable differences in resource use. The high overlap resulted mostly from all five species consuming numerous ants, a prey source that moves between microhabitats. To test the prediction that the large differences in foraging behavior explain the small dietary differences, we generated expected diets based on available prey and foraging microhabitat use. Consistent with niche partitioning as a coexistence mechanism, we found that the small dietary differences were explained by a combination of foraging microhabitat and available prey, but this pattern was driven by only a small number of prey taxa. Thus, we found mixed support for behavioral niche partitioning. Our results indicate that foraging behavior among these bird species helps explain subtle variation in diet, potentially facilitating coexistence. However, our results also revealed a weak relationship between foraging behavior and resource partitioning. Consequently, studies that rely solely on foraging behavior may greatly overestimate the degree of niche differentiation leading to erroneous conclusions. Overall, this study calls into question how and why these differences in foraging behavior evolved, and what role if any they play in facilitating coexistence.

Experimental reduction of winter food decreases body condition and delays migration in a long-distance migratory bird.

Many tropical habitats experience pronounced dry seasons, during which arthropod food availability declines, potentially limiting resident and migratory animal populations. In response to declines in food, individuals may attempt to alter their space use to enhance access to food resources, but may be socially constrained from doing so by con- and heterospecifics. If social constraints exist, food declines should result in decreased body condition. In migratory birds, correlational evidence suggests a link between body condition and migration timing. Poor body condition and delayed migration may, in turn, impact fitness in subsequent seasons via carry-over effects. To determine if winter food availability affects space use, inter- and intraspecific competition, body composition (i.e., mass, fat, and pectoral muscle), and migration timing, we experimentally decreased food availability on individual American Redstart (Setophaga ruticilla) territories in high-quality mangrove habitat. Redstarts on control territories experienced -40% loss of food due to the seasonal nature of the environment. Redstarts on experimental territories experienced -80% declines in food, which closely mimicked natural declines in nearby, low-quality, scrub habitat. Individuals on food-reduced territories did not expand their territories locally, but instead either became non-territorial "floaters" or remained on territory. Regardless of territorial status, food-reduced American Redstarts all deposited fat compared to control birds. Fat deposits provide insurance against the risk of starvation, but, for American Redstarts, came at the expense of maintaining pectoral muscle. Subsequently, food-reduced American Redstarts experienced, on average, a one-week delay in departure on spring migration, likely due to the loss of pectoral muscle. Thus, our results demonstrate experimentally, for the first time, that declines in winter food availability can result in a fat-muscle trade-off, which, in turn, delays departure on spring migration. Previous work has demonstrated that, for each day delayed after the first male arrival on the breeding grounds, American Redstarts experience an 11% decrease in the chance of successfully reproducing. Therefore, such delays in departure likely lead to fitness costs for migratory birds. Because tropical seasonal forests are expected to become drier in response to global climate change, Neotropical migratory bird populations may experience significant winter food limitation, further exacerbating population declines in the coming decades.

Non-breeding season habitat quality mediates the strength of density-dependence for a migratory bird.

Our understanding of when natural populations are regulated during their annual cycle is limited, particularly for migratory species. This information is needed for parametrizing models that can inform management and conservation. Here, we use 14 years of data on colour-marked birds to investigate how conspecific density and habitat quality during the tropical non-breeding period interact to affect body condition and apparent annual survival of a long-distance migratory songbird, the American redstart (Setophagaruticilla). Body condition and survival of birds in high-quality mangrove habitat declined as density increased. By contrast, body condition improved and survival did not vary as density increased in adjacent, lower quality scrub habitat, although mean condition and survival were almost always lower than in mangrove. High rainfall enhanced body condition in scrub but not in mangrove, suggesting factors such as food availability outweighed consequences of crowding in lower quality habitat. Thus, survival of overwintering redstarts in mangrove habitat, disproportionately males,appears to be regulated by a crowding mechanism based on density-dependent resource competition. Survival of individuals in scrub, mostly females, appears to be limited by density-independent environmental factors but not regulated by crowding. The contrasting effects of density and food limitation on individuals overwintering in adjacent habitats illustrate the complexity of processes operating during the non-breeding period for migratory animals, and emphasize the need for long-term studies of animals in multiple habitats and throughout their annual cycles.

Conserving migratory land birds in the new world: do we know enough?

Migratory bird needs must be met during four phases of the year: breeding season, fall migration, wintering, and spring migration; thus, management may be needed during all four phases. The bulk of research and management has focused on the breeding season, although several issues remain unsettled, including the spatial extent of habitat influences on fitness and the importance of habitat on the breeding grounds used after breeding. Although detailed investigations have shed light on the ecology and population dynamics of a few avian species, knowledge is sketchy for most species. Replication of comprehensive studies is needed for multiple species across a range of areas, Information deficiencies are even greater during the wintering season, when birds require sites that provide security and food resources needed for survival and developing nutrient reserves for spring migration and, possibly, reproduction. Research is needed on many species simply to identify geographic distributions, wintering sites, habitat use, and basic ecology. Studies are complicated, however, by the mobility of birds and by sexual segregation during winter. Stable-isotope methodology has offered an opportunity to identify linkages between breeding and wintering sites, which facilitates understanding the complete annual cycle of birds. The twice-annual migrations are the poorest-understood events in a bird's life. Migration has always been a risky undertaking, with such anthropogenic features as tall buildings, towers, and wind generators adding to the risk. Species such as woodland specialists migrating through eastern North America have numerous options for pausing during migration to replenish nutrients, but some species depend on limited stopover locations. Research needs for migration include identifying pathways and timetables of migration, quality and distribution of habitats, threats posed by towers and other tall structures, and any bottlenecks for migration. Issues such as human population growth, acid deposition, climate change, and exotic diseases are global concerns with uncertain consequences to migratory birds and even less-certain remedies. Despite enormous gaps in our understanding of these birds, research, much of it occurring in the past 30 years, has provided sufficient information to make intelligent conservation efforts but needs to expand to handle future challenges.

Assessing habitat quality for a migratory songbird wintering in natural and agricultural habitats.

As tropical forests are cleared, a greater proportion of migratory songbirds are forced to winter in agricultural and disturbed habitats, which, if poorer in quality than natural forests, could contribute to population declines. We compared demographic indicators of habitat quality for a focal species, the American Redstart (Setophaga ruticilla), wintering in Jamaican citrus orchards and shade coffee plantations with those in four natural habitats: mangrove, coastal scrub, coastal palm, and dry limestone forests. Demographic measures of habitat quality included density, age and sex ratio, apparent survival, and changes in body mass. Measures of habitat quality for redstarts in citrus and coffee habitats were generally intermediate between the highest (mangrove) and lowest (dry limestone) measurements from natural habitats. The decline in mean body mass over the winter period was a strong predictor of annual survival rate among habitats, and we suggest that measures of body condition coupled with survival data provide the best measures of habitat quality for nonbreeding songbirds. Density, which is far easier to estimate, was correlated with these more labor-intensive measures, particularly in the late winter when food is likely most limiting. Thus, local density may be useful as an approximation of habitat quality for wintering migrant warblers. Our findings bolster those of previous studies based on bird abundance that suggest arboreal agricultural habitats in the tropics can be useful for the conservation of generalist, insectivorous birds, including many migratory passerines such as redstarts.

Avian community response to lowland tropical rainforest isolation: 40 years of change at La Selva Biological Station, Costa Rica.

Since 1960, most of the forest surrounding the La Selva Biological Station, an intensively studied tropical research facility in Costa Rica, has been converted to agricultural uses. We used quantitative censuses and analysis of previously published categorical abundances to assess changes in the bird community, and we evaluated potential causes of species-specific changes by assessing their association with habitat, diet, participation in mixed-species flocks, and nest type. Approximately the same percentage of species increased as decreased in abundance from 1960 to 1999 (10-20% of all species, depending on method of assessment). Diet was the single most important trait associated with declining species. At least 50% of the species that declined have insectivorous diets. Use of forest habitat and participation in mixed-species flocks were also significant factors associated with declines, but nest type was unrelated to change in abundance. The species that increased in abundance tended to occur in open habitats and have omnivorous diets. These results reinforce the importance of several population risk factors associated with tropical understory insectivory and mixed-species flocking: patchy spatial distribution, low population density, large home range, and dietary specialization. La Selva's protected area (1611 ha), despite a forested connection on one boundary with a higher elevation national park, is apparently too small to maintain at least one major guild (understory insectivores). This first quantitative assessment of bird community change at La Selva highlights the need to intensify study of the mechanisms and consequences of biological diversity change in tropical forest fragments.

Food supply controls the body condition of a migrant bird wintering in the tropics.

The hypothesis that migratory bird populations are limited during the non-breeding season is increasingly supported by empirical studies that also suggest consequences that carry-over into subsequent seasons. Although variation in food supply is the best supported explanation for non-breeding season limitation, the ecological mechanisms and physiological consequences are not well understood. We both supplemented and reduced Ovenbird (Seiurus aurocapilla) food availability on replicate plots in Jamaica in each of 3 years to determine the direct role of food in limiting the physical condition of Ovenbirds. Annual variation in rainfall and food supply created a natural experiment in parallel with manipulations. Sex and age-classes of Ovenbirds did not respond differently in terms of body condition to either food manipulation or natural variation in environmental conditions, suggesting that this population is not structured by strong dominance relationships. Ovenbird body mass, fat, and pectoralis muscle shape were positively and predictably related to manipulated food availability. Feather regrowth rate also responded positively to food supplementation and negatively to food reduction in the drier of 2 years. Prior to manipulation, annual variation in body mass corresponded to annual variation in food supply and rainfall, providing additional, correlational evidence of food limitation. Since multiple intercorrelated body condition indices of Ovenbirds responded directly to food supply, and since food supply influenced body condition independently of other habitat features, we argue that food is a primary driver of non-breeding season population limitation. Moreover, since these effects were observed during the late non-breeding period, when individuals are preparing to migrate, we infer that food availability likely initiates carry-over effects.

Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird.

Identifying the factors that control population dynamics in migratory animals has been constrained by our inability to track individuals throughout the annual cycle. Using stable carbon isotopes, we show that the reproductive success of a long-distance migratory bird is influenced by the quality of habitat located thousands of kilometres away on tropical wintering grounds. For male American redstarts (Setophaga ruticilla), winter habitat quality influenced arrival date on the breeding grounds, which in turn affected key variables associated with reproduction, including the number of young fledged. Based on a winter-habitat model, females occupying high-quality winter habitat were predicted to produce more than two additional young and to fledge offspring up to a month earlier compared with females wintering in poor-quality habitat. Differences of this magnitude are highly important considering redstarts are single brooded, lay clutches of only three to five eggs and spend only two-and-a-half months on the breeding grounds. Results from this study indicate the importance of understanding how periods of the annual cycle interact for migratory animals. Continued loss of tropical wintering habitat could have negative effects on migratory populations in the following breeding season, minimizing density-dependent effects on the breeding grounds and leading to further population declines. If conservation efforts are to be successful, strategies must incorporate measures to protect all the habitats used during the entire annual cycle of migratory animals.

Bird predation on herbivorous insects: indirect effects on sugar maple saplings.

. Insectivorous birds have been shown to have direct effects on abundances of herbivorous arthropods, but few studies have tested the indirect effects of birds on plant performance through consumption of herbivorous insects. In a 3-year study at the Hubbard Brook Experimental Forest, New Hampshire, we tested whether bird predation indirectly affects leaf herbivory levels and leaf and shoot biomass production of understory sugar maple (Acer saccharum) saplings. Trees were randomly assigned to one of four treatments: an insecticide application to reduce herbivory levels, exclosures that prevented bird access, addition of Lepidoptera larvae, and controls. Trees sprayed with an insecticide supported significantly fewer Lepidoptera larvae than other treatments throughout the study. Also, trees in exclosures supported more Lepidoptera larvae than controls during one count each year, and pooled across all counts during the second year. As predicted, the mean proportion of leaf area consumed varied significantly among treatments and was least in the insecticide treatment, followed by controls, exclosures, and Lepidoptera additions. Significant differences among treatments in herbivory levels, however, did not lead to differences in leaf or shoot biomass production. Thus, bird predation decreased Lepidoptera abundances and decreased herbivory levels, but did not increase biomass production during the following year. Over 85% of the herbivores in our study were Homoptera nymphs that were not folivorous and are not important bird prey items, potentially dampening the indirect effects of bird predation on biomass production. A comparison of these results with previous studies suggests that the indirect effects of bird predation on plant biomass production may depend on the plant species, abundance and composition of the herbivore community, and primary productivity of the ecosystem.

Habitat-specific effects of food abundance on the condition of ovenbirds wintering in Jamaica.

1. Food availability has been considered one of the most important factors limiting bird populations, yet the effects of food abundance on non-breeding insectivores has rarely been investigated. We studied the effects of food abundance on the body condition of ovenbirds (Seiurus aurocapillus L.), a sexually monomorphic, ground-foraging, Neotropical-Nearctic migrant warbler during two winters in three habitats on their wintering grounds in Jamaica. 2. Prey biomass decreased from early to late winter in all habitats. Concurrently, ovenbird body mass, corrected for differences in structural size, decreased significantly in five of six habitat-year combinations. Only in second growth scrub habitat in the 1995-96 winter did ovenbirds show no decrease in corrected body mass, and during this period there was no significant decrease in ant biomass, the dominant prey item of ovenbirds in all habitats. 3. Significant positive correlations were found between ovenbirds' rate of feather regrowth and the biomass of ants on their home ranges in early winter, and between overwinter change in ovenbird body mass and the biomass of ants on their home ranges in late winter. 4. The results of both the habitat- and home-range-based analyses suggest a similar threshold of ant biomass (2·5-3·0 mg m-2 ), below which ovenbirds did not maintain their body mass. 5. The results suggest that late winter rainfall mediates the biomass of prey abundance, which in turn affects the ovenbirds' overwinter body condition.