Bethany J. Hoye

Migratory animals couple biodiversity and ecosystem functioning worldwide

Background Every year, billions of migratory animals cross the planet in pursuit of increased foraging opportunities, improved safety, and higher reproductive output. In so doing, these migrants transport nutrients, energy, and other organisms (including seeds, mollusks, parasites, and pathogens) between disparate locations. Migrants also forage and are preyed upon throughout their journeys, thereby establishing transport and trophic interactions with resident communities. Migratory animals thus couple ecological communities across the globe and may mediate their diversity and stability. However, as yet, the influence of migrants and their services on these communities is often overlooked, and as a consequence of global changes, migrations are threatened worldwide. Migrants change ecology and ecosystems. By transporting energy, nutrients, and other organisms, as well as foraging and becoming prey, migratory animals can substantially alter the dynamics of resident communities that they connect on their journeys across the globe. We illustrate key examples where migratory species profoundly alter food-web dynamics, community processes, and ecosystem functioning, indicating that migrants represent a unique, yet highly influential, component of biodiversity. Advances We review several examples in which interactions between migratory animals and resident communities have been quantified, illustrating the processes by which migrants may uniquely alter energy flow, food-web topology and stability, trophic cascades, and the structure and dynamics of (meta-)communities. For example, the inputs of nutrients and energy originating from distant localities by migrants can dramatically increase resource availability, with rippling consequences for productivity at various trophic levels and the potential to drive the transition between alternative stable states. Migrant-mediated transport of propagules of other organisms can lead to the establishment of new or lost species, as well as influencing gene flow and genetic mixing among resident populations. Similarly, migrants can alter parasite transmission, diversity, and evolution by harboring a broader range of parasites than residents and by either facilitating or hindering the long-distance dispersal of parasites. Foraging by migrants can also have profound effects on community processes and ecosystem functions. For instance, grazing by migratory animals can alter nutrient cycling, primary productivity, biomass of edible plants, competitive interactions between plant species, and ultimately, the composition and long-term persistence of the entire plant community. The most striking difference between migrant and resident consumers is, however, the pulsed nature of migrant utilization and the timing of their interactions. Together, these fundamentally define the relationship between migrant abundance and primary production (in the case of migrant herbivores) or the stability of food webs (in the case of migratory predators). Outlook Our Review demonstrates that the highly predictable, seasonally pulsed nature of animal migration, together with the spatial scales at which it operates and the immense number of individuals involved, not only set migration apart from other types of movement, but render it a uniquely potent, yet underappreciated, dimension of biodiversity that is intimately embedded within resident communities. Given the potential for migration to influence ecological networks worldwide, we suggest integrative network approaches, through which studies of community dynamics and ecosystem functioning may explicitly consider animal migrations, understand the ramifications of their declines, and assist in developing effective conservation measures. Animal migrations span the globe, involving immense numbers of individuals from a wide range of taxa. Migrants transport nutrients, energy, and other organisms as they forage and are preyed upon throughout their journeys. These highly predictable, pulsed movements across large spatial scales render migration a potentially powerful yet underappreciated dimension of biodiversity that is intimately embedded within resident communities. We review examples from across the animal kingdom to distill fundamental processes by which migratory animals influence communities and ecosystems, demonstrating that they can uniquely alter energy flow, food-web topology and stability, trophic cascades, and the structure of metacommunities. Given the potential for migration to alter ecological networks worldwide, we suggest an integrative framework through which community dynamics and ecosystem functioning may explicitly consider animal migrations. Migration Monitor Seasonal migrations move large numbers of animals across often vast distances. Such movement shifts large amounts of biomass from one region to another, but, perhaps more importantly, moves animals that eat, excrete, and sometimes die in multiple remote systems. Such movements impact the communities, trophic structure, and function of these ecosystems in often underappreciated ways. Bauer and Hoye (10.1126/science.1242552) review migrations across taxa to identify the key ecological roles these long-distance movements play, and the unique threats the animals face in our increasingly modified world.

Surveillance of wild birds for avian influenza virus

TOC Summary: A targeted, hypothesis-based approach and local surveys over broad geographic areas are needed.

Ecophysiology of avian migration in the face of current global hazards

Long-distance migratory birds are often considered extreme athletes, possessing a range of traits that approach the physiological limits of vertebrate design. In addition, their movements must be carefully timed to ensure that they obtain resources of sufficient quantity and quality to satisfy their high-energy needs. Migratory birds may therefore be particularly vulnerable to global change processes that are projected to alter the quality and quantity of resource availability. Because long-distance flight requires high and sustained aerobic capacity, even minor decreases in vitality can have large negative consequences for migrants. In the light of this, we assess how current global change processes may affect the ability of birds to meet the physiological demands of migration, and suggest areas where avian physiologists may help to identify potential hazards. Predicting the consequences of global change scenarios on migrant species requires (i) reconciliation of empirical and theoretical studies of avian flight physiology; (ii) an understanding of the effects of food quality, toxicants and disease on migrant performance; and (iii) mechanistic models that integrate abiotic and biotic factors to predict migratory behaviour. Critically, a multi-dimensional concept of vitality would greatly facilitate evaluation of the impact of various global change processes on the population dynamics of migratory birds.

Juveniles and migrants as drivers for seasonal epizootics of avian influenza virus

Similar to other infectious diseases, the prevalence of low pathogenic avian influenza viruses (LPAIV) has been seen to exhibit marked seasonal variation. However, mechanisms driving this variation in wild birds have yet to be tested. We investigated the validity of three previously suggested drivers for the seasonal dynamics in LPAIV infections in wild birds: (i) host density, (ii) immunologically naïve young and (iii) increased susceptibility in migrants. To address these questions, we sampled a key LPAIV host species, the mallard Anas platyrhynchos, on a small spatial scale, comprehensively throughout a complete annual cycle, measuring both current and past infection (i.e. viral and seroprevalence, respectively). We demonstrate a minor peak in LPAIV prevalence in summer, a dominant peak in autumn, during which half of the sampled population was infected, and no infections in spring. Seroprevalence of antibodies to a conserved gene segment of avian influenza virus (AIV) peaked in winter and again in spring. The summer peak of LPAIV prevalence coincided with the entrance of unfledged naïve young in the population. Moreover, juveniles were more likely to be infected, shed higher quantities of virus and were less likely to have detectable antibodies to AIV than adult birds. The arrival of migratory birds, as identified by stable hydrogen isotope analysis, appeared to drive the autumn peak in LPAIV infection, with both temporal coincidence and higher infection prevalence in migrants. Remarkably, seroprevalence in migrants was substantially lower than viral prevalence throughout autumn migration, further indicating that each wave of migrants amplified local AIV circulation. Finally, while host abundance increased throughout autumn, it peaked in winter, showing no direct correspondence with either of the LPAIV infection peaks. At an epidemiologically relevant spatial scale, we provide strong evidence for the role of migratory birds as key drivers for seasonal epizootics of LPAIV, regardless of their role as vectors of these viruses. This study exemplifies the importance of understanding host demography and migratory behaviour when examining seasonal drivers of infection in wildlife populations.

From Food to Offspring Down: Tissue-Specific Discrimination and Turn-Over of Stable Isotopes in Herbivorous Waterbirds and Other Avian Foraging Guilds

Isotopic discrimination and turn-over are fundamental to the application of stable isotope ecology in animals. However, detailed information for specific tissues and species are widely lacking, notably for herbivorous species. We provide details on tissue-specific carbon and nitrogen discrimination and turn-over times from food to blood, feathers, claws, egg tissues and offspring down feathers in four species of herbivorous waterbirds. Source-to-tissue discrimination factors for carbon (δ13C) and nitrogen stable isotope ratios (δ15N) showed little variation across species but varied between tissues. Apparent discrimination factors ranged between −0.5 to 2.5‰ for δ13C and 2.8 to 5.2‰ for δ15N, and were more similar between blood components than between keratinous tissues or egg tissue. Comparing these results with published data from other species we found no effect of foraging guild on discrimination factors for carbon but a significant foraging-guild effect for nitrogen discrimination factors. Turn-over of δ13C in tissues was most rapid in blood plasma, with a half-life of 4.3 d, whereas δ13C in blood cells had a half-life of approximately 32 d. Turn-over times for albumen and yolk in laying females were similar to those of blood plasma, at 3.2 and 6.0 d respectively. Within yolk, we found decreasing half-life times of δ13C from inner yolk (13.3 d) to outer yolk (3.1 d), related to the temporal pattern of tissue formation. We found similarities in tissue-specific turn-over times across all avian species studied to date. Yet, while generalities regarding discrimination factors and tissue turn-over times can be made, a large amount of variation remains unexplained.

How to find natural reservoir hosts from endemic prevalence in a multi-host population: a case study of influenza in waterfowl.

The transmission dynamics of infectious diseases critically depend on reservoir hosts, which can sustain the pathogen (or maintain the transmission) in the population even in the absence of other hosts. Although a theoretical foundation of the transmission dynamics in a multi-host population has been established, no quantitative methods exist for the identification of natural reservoir hosts. For a host to maintain the transmission alone, the host-specific reproduction number (U), interpreted as the average number of secondary transmissions caused by a single primary case in the host(s) of interest in the absence of all other hosts, must be greater than unity. If the host-excluded reproduction number (Q), representing the average number of secondary transmissions per single primary case in other hosts in the absence of the host(s) of interest, is below unity, transmission cannot be maintained in the multi-host population in the absence of the focal host(s). The present study proposes a simple method for the identification of reservoir host(s) from observed endemic prevalence data across a range of host species. As an example, we analyze an aggregated surveillance dataset of influenza A virus in wild birds among which dabbling ducks exhibit higher prevalence compared to other bird species. Since the heterogeneous contact patterns between different host species are not directly observable, we test four different contact structures to account for the uncertainty. Meeting the requirements of U>1 and Q<1 for all four different contact structures, mallards and other dabbling ducks most likely constitute the reservoir community which plays a predominant role in maintaining the transmission of influenza A virus in the water bird population. We further discuss epidemiological issues which are concerned with the interpretation of influenza prevalence data, identifying key features to be fully clarified in the future.

Host behaviour and physiology underpin individual variation in avian influenza virus infection in migratory Bewick's swans

Individual variation in infection modulates both the dynamics of pathogens and their impact on host populations. It is therefore crucial to identify differential patterns of infection and understand the mechanisms responsible. Yet our understanding of infection heterogeneity in wildlife is limited, even for important zoonotic host–pathogen systems, owing to the intractability of host status prior to infection. Using novel applications of stable isotope ecology and eco-immunology, we distinguish antecedent behavioural and physiological traits associated with avian influenza virus (AIV) infection in free-living Bewicks swans (Cygnus columbianus bewickii). Swans infected with AIV exhibited higher serum δ13C (−25.3 ± 0.4) than their non-infected counterparts (−26.3 ± 0.2). Thus, individuals preferentially foraging in aquatic rather than terrestrial habitats experienced a higher risk of infection, suggesting that the abiotic requirements of AIV give rise to heterogeneity in pathogen exposure. Juveniles were more likely to be infected (30.8% compared with 11.3% for adults), shed approximately 15-fold higher quantity of virus and exhibited a lower specific immune response than adults. Together, these results demonstrate the potential for heterogeneity in infection to have a profound influence on the dynamics of pathogens, with concomitant impacts on host habitat selection and fitness.

Effects of infection-induced migration delays on the epidemiology of avian influenza in wild mallard populations.

Wild waterfowl populations form a natural reservoir of Avian Influenza (AI) virus, and fears exist that these birds may contribute to an AI pandemic by spreading the virus along their migratory flyways. Observational studies suggest that individuals infected with AI virus may delay departure from migratory staging sites. Here, we explore the epidemiological dynamics of avian influenza virus in a migrating mallard (Anas platyrhynchos) population with a specific view to understanding the role of infection-induced migration delays on the spread of virus strains of differing transmissibility. We develop a host-pathogen model that combines the transmission dynamics of influenza with the migration, reproduction and mortality of the host bird species. Our modeling predicts that delayed migration of individuals influences both the timing and size of outbreaks of AI virus. We find that (1) delayed migration leads to a lower total number of cases of infection each year than in the absence of migration delay, (2) when the transmission rate of a strain is high, the outbreak starts at the staging sites at which birds arrive in the early part of the fall migration, (3) when the transmission rate is low, infection predominantly occurs later in the season, which is further delayed when there is a migration delay. As such, the rise of more virulent AI strains in waterfowl could lead to a higher prevalence of infection later in the year, which could change the exposure risk for farmed poultry. A sensitivity analysis shows the importance of generation time and loss of immunity for the effect of migration delays. Thus, we demonstrate, in contrast to many current transmission risk models solely using empirical information on bird movements to assess the potential for transmission, that a consideration of infection-induced delays is critical to understanding the dynamics of AI infection along the entire flyway.

Inexplicable inefficiency of avian molt? Insights from an opportunistically breeding arid-zone species, Lichenostomus penicillatus.

The majority of bird species studied to date have molt schedules that are not concurrent with other energy demanding life history stages, an outcome assumed to arise from energetic trade-offs. Empirical studies reveal that molt is one of the most energetically demanding and perplexingly inefficient growth processes measured. Furthermore, small birds, which have the highest mass-specific basal metabolic rates (BMRm), have the highest costs of molt per gram of feathers produced. However, many small passerines, including white-plumed honeyeaters (WPHE; Lichenostomus penicillatus), breed in response to resource availability at any time of year, and do so without interrupting their annual molt. We examined the energetic cost of molt in WPHE by quantifying weekly changes in minimum resting metabolic rate (RMRmin) during a natural-molt period in 7 wild-caught birds. We also measured the energetic cost of feather replacement in a second group of WPHEs that we forced to replace an additional 25% of their plumage at the start of their natural molt period. Energy expenditure during natural molt revealed an energy conversion efficiency of just 6.9% (±0.57) close to values reported for similar-sized birds from more predictable north-temperate environments. Maximum increases in RMRmin during the molt of WPHE, at 82% (±5.59) above individual pre-molt levels, were some of the highest yet reported. Yet RMRmin maxima during molt were not coincident with the peak period of feather replacement in naturally molting or plucked birds. Given the tight relationship between molt efficiency and mass-specific metabolic rate in all species studied to date, regardless of life-history pattern (Efficiency (%)  = 35.720•10−0.494BMRm; r2 = 0.944; p = <0.0001), there appears to be concomitant physiological costs entrained in the molt period that is not directly due to feather replacement. Despite these high total expenditures, the protracted molt period of WPHE significantly reduces these added costs on a daily basis.

Habitat use throughout migration: linking individual consistency, prior breeding success and future breeding potential

1. Habitat use can influence individual performance in a wide range of animals, either immediately or through carry-over effects in subsequent seasons. Given that many animal species also show consistent individual differences in reproductive success, it seems plausible that individuals may have consistent patterns of habitat use representing individual specializations, with concomitant fitness consequences. 2. Stable-carbon isotope ratios from a range of tissues were used to discern individual consistency in habitat use along a terrestrial-aquatic gradient in a long-distance migrant, the Bewicks swan (Cygnus columbianus bewickii). These individual specialisations represented <15% of the isotopic breadth of the population for the majority of individuals and were seen to persist throughout autumn migration and overwintering until aquatic habitats were no longer available. 3. Individual foraging specialisations were then used to demonstrate two consecutive carry-over effects associated with macroscale habitat segregation: consequences of breeding season processes for autumn habitat use; and consequences of autumn habitat use for future reproductive success. Adults that were successful breeders in the year of capture used terrestrial habitats significantly more than adults that were not successful, revealing a substantial cost of reproduction and extended parental care. Use of aquatic habitats during autumn was, however, associated with increased body condition prior to spring migration; and increased subsequent breeding success in adults that had been unsuccessful the year before. Yet adults that were successful breeders in the year of capture remained the most likely to be successful the following year, despite their use of terrestrial habitats. 4. Our results uniquely demonstrate not only individual foraging specializations throughout the migration period, but also that processes during breeding and autumn migration, mediated by individual consistency, may play a fundamental role in the population dynamics of long-distance migrants. These findings, therefore, highlight the importance of long-term consistency to our understanding of habitat function, interindividual differences in fitness, population dynamics and the evolution of migratory strategies.