Peter P. Marra

Links between worlds: unraveling migratory connectivity

Migration is the regular seasonal movement of animals from one place to another, often from a breeding site to a nonbreeding site and back. Because the act of migration makes it difficult to follow individuals and populations year round, our understanding of the ecology and evolution of migrating organisms, particularly birds, has been severely impeded. Exciting new advances in satellite telemetry, genetic analyses and stable isotope chemistry are now making it possible to determine the population and geographical origin of individual birds. Here, we review these new approaches and consider the relevance of understanding migratory connectivity to ecological, evolutionary and conservation issues.

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.

Predicting the global spread of H5N1 avian influenza

The spread of highly pathogenic H5N1 avian influenza into Asia, Europe, and Africa has resulted in enormous impacts on the poultry industry and presents an important threat to human health. The pathways by which the virus has and will spread between countries have been debated extensively, but have yet to be analyzed comprehensively and quantitatively. We integrated data on phylogenetic relationships of virus isolates, migratory bird movements, and trade in poultry and wild birds to determine the pathway for 52 individual introduction events into countries and predict future spread. We show that 9 of 21 of H5N1 introductions to countries in Asia were most likely through poultry, and 3 of 21 were most likely through migrating birds. In contrast, spread to most (20/23) countries in Europe was most likely through migratory birds. Spread in Africa was likely partly by poultry (2/8 introductions) and partly by migrating birds (3/8). Our analyses predict that H5N1 is more likely to be introduced into the Western Hemisphere through infected poultry and into the mainland United States by subsequent movement of migrating birds from neighboring countries, rather than from eastern Siberia. These results highlight the potential synergism between trade and wild animal movement in the emergence and pandemic spread of pathogens and demonstrate the value of predictive models for disease control.

West Nile Virus Epidemics in North America Are Driven by Shifts in Mosquito Feeding Behavior

West Nile virus (WNV) has caused repeated large-scale human epidemics in North America since it was first detected in 1999 and is now the dominant vector-borne disease in this continent. Understanding the factors that determine the intensity of the spillover of this zoonotic pathogen from birds to humans (via mosquitoes) is a prerequisite for predicting and preventing human epidemics. We integrated mosquito feeding behavior with data on the population dynamics and WNV epidemiology of mosquitoes, birds, and humans. We show that Culex pipiens, the dominant enzootic (bird-to-bird) and bridge (bird-to-human) vector of WNV in urbanized areas in the northeast and north-central United States, shifted its feeding preferences from birds to humans by 7-fold during late summer and early fall, coinciding with the dispersal of its preferred host (American robins, Turdus migratorius) and the rise in human WNV infections. We also show that feeding shifts in Cx. tarsalis amplify human WNV epidemics in Colorado and California and occur during periods of robin dispersal and migration. Our results provide a direct explanation for the timing and intensity of human WNV epidemics. Shifts in feeding from competent avian hosts early in an epidemic to incompetent humans after mosquito infection prevalences are high result in synergistic effects that greatly amplify the number of human infections of this and other pathogens. Our results underscore the dramatic effects of vector behavior in driving the transmission of zoonotic pathogens to humans.

West Nile virus emergence and large-scale declines of North American bird populations

Emerging infectious diseases present a formidable challenge to the conservation of native species in the twenty-first century. Diseases caused by introduced pathogens have had large impacts on species abundances, including the American chestnut, Hawaiian bird species and many amphibians. Changes in host population sizes can lead to marked shifts in community composition and ecosystem functioning. However, identifying the impacts of an introduced disease and distinguishing it from other forces that influence population dynamics (for example, climate) is challenging and requires abundance data that extend before and after the introduction. Here we use 26 yr of Breeding Bird Survey (BBS) data to determine the impact of West Nile virus (WNV) on 20 potential avian hosts across North America. We demonstrate significant changes in population trajectories for seven species from four families that concur with a priori predictions and the spatio-temporal intensity of pathogen transmission. The American crow population declined by up to 45% since WNV arrival, and only two of the seven species with documented impact recovered to pre-WNV levels by 2005. Our findings demonstrate the potential impacts of an invasive species on a diverse faunal assemblage across broad geographical scales, and underscore the complexity of subsequent community response.

Host heterogeneity dominates West Nile virus transmission

Heterogeneity in host populations and communities can have large effects on the transmission and control of a pathogen. In extreme cases, a few individuals give rise to the majority of secondary infections, which have been termed super spreading events. Here, we show that transmission of West Nile virus (WNV) is dominated by extreme heterogeneity in the host community, resulting in highly inflated reproductive ratios. A single relatively uncommon avian species, American robin (Turdus migratorius), appeared to be responsible for the majority of WNV-infectious mosquitoes and acted as the species equivalent of a super spreader for this multi-host pathogen. Crows were also highly preferred by mosquitoes at some sites, while house sparrows were significantly avoided. Nonetheless, due to their relative rarity, corvids (crows and jays) were relatively unimportant in WNV amplification. These results challenge current beliefs about the role of certain avian species in WNV amplification and demonstrate the importance of determining contact rates between vectors and host species to understand pathogen transmission dynamics.

Corticosterone levels as indicators of habitat quality: effects of habitat segregation in a migratory bird during the non-breeding season

Abstract During the non-breeding season, many species of territorial migratory birds exhibit a non-random pattern of habitat distribution, with males and females occupying different habitats. In this study, we examined possible physiological consequences arising from such habitat segregation in one migrant passerine species, the American redstart (Setophaga ruticilla), on its non-breeding grounds in Jamaica, West Indies. For 2 years, we measured concentrations of corticosterone, at the time of capture (baseline) and 30 min after capture (profile of acute corticosterone secretion), in redstarts in two distinct habitats, one occupied predominately by males and one mostly by females. All redstarts in both habitat types exhibited similar concentrations of baseline corticosterone levels in fall (October), whereas in spring (March–April), redstarts in female-biased habitat exhibited significantly higher baseline levels regardless of age or sex. In fall, all individuals in both habitats exhibited significant increases in corticosterone concentration with capture and handling, but in spring only redstarts (both sexes) in male-biased habitat continued to exhibit acute corticosterone secretion. Redstarts in female-biased habitat had elevated baseline corticosterone levels and reduced acute corticosterone secretion. In spring, baseline corticosterone concentration was negatively correlated with body mass, suggesting muscle catabolism associated with high corticosterone concentrations or possibly that birds are leaner as a result of increased foraging effort. These results indicate that redstarts (primarily females) in female-biased habitats suffered a decline in physiological condition, which could in turn influence their departure schedules, migration patterns and even their condition and arrival schedules on the breeding grounds. Thus, segregation of populations into habitats of different quality during the non-breeding period may have ramifications throughout the annual cycle of such migratory species. Furthermore, these results show the usefulness of plasma corticosterone levels as indicators of physiological condition and thus habitat quality for birds during the non-breeding period.

Habitat-specific demography of breeding black-throated blue warblers (Dendroica caerulescens) : implications for populations dynamics

The distribution of individuals among habitats and their relative success in those habitats can have important consequences for population dynamics. To examine these processes for a long-distance migratory bird species, we studied the population structure, age-specific reproductive output, and local survival of black-throated blue warblers (Dendroica caerulescens, Gmelin) in two breeding habitats differing in shrub density within northern hardwoods forests in New Hampshire, USA. On forest plots with dense shrubs, warblers occurred at higher densities, and fledged significantly more young per capita per season than those occupying areas with lower shrub density. This differential productivity was due to higher reproductive output, mainly through double-brooding, of older (≥ 2 years of age) individuals, which were disproportionately more abundant in high shrub density sites. Clutch initiation dates, clutch sizes, and predation rates at individual nests did not differ significantly between habitats. Mean body mass of nestlings on day 6 following hatching were higher on average on plots with high shrub density, but differences were not significant. Annual return rates, as indices of local survival, did not differ between habitats for older males or for females. Yearling males, however, returned in subsequent years at a significantly lower rate to low shrub density plots, a result of either lower survival or, more likely, dispersal to more suitable habitat in their second year of breeding. Parental age and habitat suitability interact in that older individuals, through their experience and/or dominance, acquire sites of higher quality, which results in higher reproductive output and probably higher survival. These differences between habitats in density, reproductive performance and local survival are consistent with an ideal-despotic/preemptive distribution of individuals, and suggest that this population could be regulated by the availability, distribution, and extent of high and low quality breeding habitats.

The impact of free-ranging domestic cats on wildlife of the United States

Anthropogenic threats, such as collisions with man-made structures, vehicles, poisoning and predation by domestic pets, combine to kill billions of wildlife annually. Free-ranging domestic cats have been introduced globally and have contributed to multiple wildlife extinctions on islands. The magnitude of mortality they cause in mainland areas remains speculative, with large-scale estimates based on non-systematic analyses and little consideration of scientific data. Here we conduct a systematic review and quantitatively estimate mortality caused by cats in the United States. We estimate that free-ranging domestic cats kill 1.4-3.7 billion birds and 6.9-20.7 billion mammals annually. Un-owned cats, as opposed to owned pets, cause the majority of this mortality. Our findings suggest that free-ranging cats cause substantially greater wildlife mortality than previously thought and are likely the single greatest source of anthropogenic mortality for US birds and mammals. Scientifically sound conservation and policy intervention is needed to reduce this impact.

Optimal conservation of migratory species.

Background Migratory animals comprise a significant portion of biodiversity worldwide with annual investment for their conservation exceeding several billion dollars. Designing effective conservation plans presents enormous challenges. Migratory species are influenced by multiple events across land and sea–regions that are often separated by thousands of kilometres and span international borders. To date, conservation strategies for migratory species fail to take into account how migratory animals are spatially connected between different periods of the annual cycle (i.e. migratory connectivity) bringing into question the utility and efficiency of current conservation efforts. Methodology/Principal Findings Here, we report the first framework for determining an optimal conservation strategy for a migratory species. Employing a decision theoretic approach using dynamic optimization, we address the problem of how to allocate resources for habitat conservation for a Neotropical-Nearctic migratory bird, the American redstart Setophaga ruticilla, whose winter habitat is under threat. Our first conservation strategy used the acquisition of winter habitat based on land cost, relative bird density, and the rate of habitat loss to maximize the abundance of birds on the wintering grounds. Our second strategy maximized bird abundance across the entire range of the species by adding the constraint of maintaining a minimum percentage of birds within each breeding region in North America using information on migratory connectivity as estimated from stable-hydrogen isotopes in feathers. We show that failure to take into account migratory connectivity may doom some regional populations to extinction, whereas including information on migratory connectivity results in the protection of the species across its entire range. Conclusions/Significance We demonstrate that conservation strategies for migratory animals depend critically upon two factors: knowledge of migratory connectivity and the correct statement of the conservation problem. Our framework can be used to identify efficient conservation strategies for migratory taxa worldwide, including insects, birds, mammals, and marine organisms.