The ecology of emerging infectious diseases in migratory birds: an assessment of the role of climate change and priorities for future research

Pathogens that are maintained by wild birds occasionally jump to human hosts, causing considerable loss of life and disruption to global commerce. Preliminary evidence suggests that climate change and human movements and commerce may have played a role in recent range expansions of avian pathogens. Since the magnitude of climate change in the coming decades is predicted to exceed climatic changes in the recent past, there is an urgent need to determine the extent to which climate change may drive the spread of disease by avian migrants. In this review, we recommend actions intended to mitigate the impact of emergent pathogens of migratory birds on biodiversity and public health. Increased surveillance that builds upon existing bird banding networks is required to conclusively establish a link between climate and avian pathogens and to prevent pathogens with migratory bird reservoirs from spilling over to humans.     

Flying with diverse passengers: greater richness of parasitic nematodes in migratory birds

Environmental changes are simultaneously affecting parasitic diseases and animal migrations, making it important to understand the disease dynamics of migratory species, including their range of infections and investment into defences. There is an urgent need for such knowledge because migratory animals, especially birds, are important for pathogen transmission and also particularly sensitive to environmental changes. Here we compare the nematode species richness and relative immune investment (via relative spleen size) of almost 200 migratory and non‐migratory species within three diverse groups of birds (Anseriformes, Accipitriformes and Turdidae) with worldwide distributions and varied ecology. Our results provide the first large‐scale demonstration that migratory birds face greater challenge from macroparasites as they have significantly dissimilar nematode fauna and higher nematode species richness compared to non‐migratory species. Even though birds with relatively large spleens had more nematode species, there was no difference in relative spleen size between migratory and non‐migratory bird species. The physiological stress of migration can be exacerbated by the potential range of pathologies induced by their richer nematode communities, particularly in combination with environmental perturbations. Altered migration stemming from global changes can also have important consequences for nematode transmission. Synthesis Most studies on parasites of migratory birds versus non‐migratory birds focus upon blood parasites; here we compared the diversity of another important parasite group – nematodes (roundworms) in three orders of birds. We found for any given order, migratory species and species with proportionally larger spleens generally have a wider range of nematodes. It is unclear why migratory species harbour more nematode species. Global climate change is expected to influence both bird migration patterns and infectious diseases, which may increase host susceptibility to parasitism and also introduce diverse nematodes to new areas and potential hosts.     

Why fly the extra mile? Using stress biomarkers to assess wintering habitat quality in migratory shorebirds

Migratory birds make decisions about how far to travel based on cost-benefit trade-offs. However, in many cases the net effect of these trade-offs is unclear. We sought to address this question by measuring feather corticosterone (CORT_f), leucocyte profile, avian malaria parasite prevalence and estimating fueling rates in three spatially segregated wintering populations of the migratory shorebird ruddy turnstone Arenaria interpres during their stay in the winter habitat. These birds fly from the high-Arctic breeding ground to Australia, but differ in that some decide to end their migration early (Broome, Western Australia), whereas others travel further to either South Australia or Tasmania. We hypothesized that the extra costs in birds migrating greater distances and overwintering in colder climates would be offset by benefits when reaching their destination. This would be evidenced by lower stress biomarkers in populations that travel further, owing to the expected benefits of greater resources and improved vitality. We show that avian malaria prevalence and physiological stress levels were lower in birds flying to South Australia and Tasmania than those overwintering in Broome. Furthermore, our modeling predicts that birds in the southernmost locations enjoy higher fueling rates. Our data are consistent with the interpretation that birds occupying more costly wintering locations in terms of higher migratory flight and thermoregulatory costs are compensated by better feeding conditions and lower blood parasite infections, which facilitates timely and speedy migration back to the breeding ground. These data contribute to our understanding of cost-benefit trade-offs in the decision making underlying migratory behaviour.     

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

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. Received: 14 November 1997 / Accepted: 9 March 1998     

The disproportionate effect of global warming on the arrival dates of short-distance migratory birds in North America

Recent studies have shown that, in response to global climate change, diverse avian taxa are now nesting measurably earlier (< 10 days) in both the United States and Britain. Similarly, several studies on European birds have now demonstrated that a variety of species (although not all) are arriving increasingly early. However, surprisingly, widespread changes in North American migrant phenology have not been demonstrated. It is hypothesized that short-distance migrants (birds that winter in the southern United States) may be quicker to adapt to climate change than long-distance migrants (birds that winter south of the United States), as short-distance migrants can respond to meteorological cues indicating weather conditions to the north whereas long-distance migrants must rely on photoperiod. This study examined the first arrival dates of 103 migrant birds in New York and Massachusetts and found that, on average, all migrants arrived significantly earlier during the period 1951–1993 than the period 1903–1950. From 1951–1993 birds wintering in the southern United States arrived on average 13 days earlier while birds wintering in South America arrived 4 days earlier. Although a change in observer effort cannot be quantified and may be a source of bias, a comparison of the numbers of reporting observers during the 1930s and the 1980s revealed no significant difference. These results are consistent with those expected under a scenario of global warming.     

Local temperature fine-tunes the timing of spring migration in birds

Evidence for climate-driven phenological changes is rapidly increasing at all trophic levels. Our current poor knowledge of the detailed control of bird migration from the level of genes and hormonal control to direct physiological and behavioral responses hampers our ability to understand and predict consequences of climatic change for migratory birds. In order to better understand migration phenology and adaptation in environmental changes, we here assess the scale at which weather affects timing of spring migration in passerine birds. We use three commonly used proxies of spring-time climatic conditions: (1) vegetation "greenness" (NDVI) in Europe, (2) local spring temperatures in northern Europe, and (3) the North Atlantic Oscillation Index (NAO) as predictors of the phenology of avian migration as well as the strength of their effect on different subsets of populations and the dependence of correlations on species-specific migratory strategy. We analyze phenological patterns of the entire spring migration period in 12 Palaearctic passerine species, drawing on long-term data collected at three locations along a longitudinal gradient situated close to their northern European breeding area. Local temperature was the best single predictor of phenology with the highest explanatory power achieved in combination with NAO. Furthermore, early individuals are more affected by climatic variation compared to individuals on later passage, indicating that climatic change affects subsets of migratory populations differentially. Species wintering closer to the breeding areas were affected more than were those travelling longer distances and this pattern was strongest for the earliest subsets of the population. Overall, our results suggest that at least early subsets of the population are affected by local conditions and early birds use local conditions to fine-tune the date of their spring arrival while individuals arriving later are driven by other factors than local conditions e.g. endogenous control. Understanding what cues migratory organisms use to arrive at an optimum time is important for increasing our knowledge of fundamental issues like decision making in organisms during migration and is crucial for future protection of migratory organisms.     

Swainson’s thrushes in migratory disposition exhibit reduced immune function

Evidence indicates that the immune system, which protects an organism from parasitic and pathogenic infections, is frequently suppressed when animals are engaged in activities involving strenuous exercise. We tested the hypothesis that birds reduce immune function during the migratory period in preparation for the anticipated heightened energetic demands of long flights. Swainson’s thrushes (Catharus ustulatus), captured in fall, were held in an indoor aviary until January, when migratory disposition was induced in half of the birds with an artificially prolonged daylength. Experimental birds became hyperphagic and deposited fat stores, and then displayed nocturnal activity (Zugunruhe) characteristic of the spring migratory period. Cell-mediated immunity was measured by intradermal injection of phytohemagglutinin in the wing patagium of both control and experimental birds. Birds exhibiting migratory restlessness had a reduced cell-mediated immune response compared to control birds. Our results suggest that birds are immunosuppressed during the migratory period. The suppression may be a nonadaptive response due to unrelated physiological processes, or it may be an adaptive response to the physiological demands associated with migration, such as high energetic demands and the negative consequences of a hyperactive immune system.     

Mapping Global Diversity Patterns for Migratory Birds

Nearly one in five bird species has separate breeding and overwintering distributions, and the regular migrations of these species cause a substantial seasonal redistribution of avian diversity across the world. However, despite its ecological importance, bird migration has been largely ignored in studies of global avian biodiversity, with few studies having addressed it from a macroecological perspective. Here, we analyse a dataset on the global distribution of the world’s birds in order to examine global spatial patterns in the diversity of migratory species, including: the seasonal variation in overall species diversity due to migration; the contribution of migratory birds to local bird diversity; and the distribution of narrow-range and threatened migratory birds. Our analyses reveal a striking asymmetry between the Northern and Southern hemispheres, evident in all of the patterns investigated. The highest migratory bird diversity was found in the Northern Hemisphere, with high inter-continental turnover in species composition between breeding and non-breeding seasons, and extensive regions (at high latitudes) where migratory birds constitute the majority of the local avifauna. Threatened migratory birds are concentrated mainly in Central and Southern Asia, whereas narrow-range migratory species are mainly found in Central America, the Himalayas and Patagonia. Overall, global patterns in the diversity of migratory birds indicate that bird migration is mainly a Northern Hemisphere phenomenon. The asymmetry between the Northern and Southern hemispheres could not have easily been predicted from the combined results of regional scale studies, highlighting the importance of a global perspective.     

Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance

Birds during migration must satisfy the high energy and nutrient demands associated with repeated, intensive flight while often experiencing unpredictable variation in food supply and food quality. Solutions to such different challenges may often be physiologically incompatible. For example, increased food intake and gut size are primarily responsible for satisfying the high energy and nutrient demands associated with migration in birds. However, short-term fasting or food restriction during flight may cause partial atrophy of the gut that may limit utilization of ingested food energy and nutrients. We review the evidence available on the effects of long- and short-term changes in food quality and quantity on digestive performance in migratory birds, and the importance of digestive constraints in limiting the tempo of migration in birds. Another important physiological consequence of feeding in birds is the effect of diet on body composition dynamics during migration. Recent evidence suggests that birds utilize and replenish both protein and fat reserves during migration, and diet quality influences the rate of replenishment of both these reserves. We conclude that diet and phenotypic flexibility in both body composition and the digestive system of migratory birds are important in allowing birds to successfully overcome the often-conflicting physiological challenges of migration.     

Two different types of light-dependent responses to magnetic fields in birds

A model of magnetoreception proposes that the avian magnetic compass is based on a radical pair mechanism, with photon absorption leading to the formation of radical pairs. Analyzing the predicted light dependency by testing migratory birds under monochromatic lights, we found that the responses of birds change with increasing intensity. The analysis of the orientation of European robins under 502 nm turquoise light revealed two types of responses depending on light intensity: under a quantal flux of 8.10(15) quanta m(-2) s(-1), the birds showed normal migratory orientation in spring as well as in autumn, relying on their inclination compass. Under brighter light of 54.10(15) quanta m(-2) s(-1), however, they showed a "fixed" tendency toward north that did not undergo the seasonal change and proved to be based on magnetic polarity, not involving the inclination compass. When birds were exposed to a weak oscillating field, which specifically interferes with radical pair processes, the inclination compass response was disrupted, whereas the response to magnetic polarity remained unaffected. These findings indicate that the normal inclination compass used for migratory orientation is based on a radical-pair mechanism, whereas the fixed direction represents a novel type of light-dependent orientation based on a mechanism of a different nature.     

‘Chancing on a spectacle:’ co-occurring animal migrations and interspecific interactions

Migrations of diverse wildlife species often converge in space and time, with their journeys shaped by similar forces (i.e. geographic barriers and seasonal resources and conditions); we term this ‘co-migration’. Recent studies have illuminated multi-speciesmigrations by land and sea including the simultaneous movements of numerous insects, birds, bats and of fish invertebrates marine predators. Beyond their significance as natural wonders, species with overlapping migrations may interact ecologically, with potential effects on population and community dynamics. Direct and indirect ecological interactions (including predation and competition) between migrant species remain poorly understood, in part because migration is the least-studied phase of animals’ annual cycles. To address this gap, we conducted a literature review to examine whether animal migration studies incorporate multiple species and to what extent they investigate interspecific interactions between co-migrants. Following a key word search, we read all migration research papers in 23 relevant peer-reviewed journals during 2008–2017. Thirty percent of animal migration papers reported two or more species with coinciding migrations, suggesting that co-migrations are common, although few studies investigated or discussed these mixed-species migrations further. Synthesizing these, we present examples and describe five types of ecological interactions between migrating species, including predator–prey, host–parasite and commensal relationships. Considering migratory animals as interacting with migrant communities will enhance understanding of the drivers of migration and could improve predictions about wildlife responses to global change. Further research focused on multi-species migrations could also inform conservation efforts for migratory animal populations, many of which are declining or shifting, with unexplored consequences for other co-migratory species.     

Recent expansion of highly pathogenic avian influenza H5N1: a critical review

Wild birds, particularly waterfowl, are a key element of the viral ecology of avian influenza. Highly pathogenic avian influenza (HPAI) virus, subtype H5N1, was first detected in poultry in November 1996 in southeast China, where it originated. The virus subsequently dispersed throughout most of Asia, and also to Africa and Europe. Despite compelling evidence that the virus has been dispersed widely via human activities that include farming, and marketing of poultry, migratory birds have been widely considered to be the primary source of its global dispersal. Here we present a critical examination of the arguments both for and against the role of migratory birds in the global dispersal of HPAI H5N1. We conclude that, whilst wild birds undoubtedly contribute to the local spread of the virus in the wild, human commercial activities, particularly those associated with poultry, are the major factors that have determined its global dispersal.     

Wing and leg bone microstructure reflects migratory demands in resident and migrant populations of the Dark-eyed Junco (Junco hyemalis)

Migration is the primary strategy that temperate birds use to avoid overwintering under harsh conditions. As a consequence, migratory birds have evolved specific morphological features in their wings and skeleton. However, in addition to varying in overall shape and size, bone can also change at the microstructural level by, for example, increasing its thickness. Such changes are critical to preventing fracture and damage under repeated loading (fatigue), yet it is not known whether migratory behaviour influences bone microstructure. To address this gap in the literature, we performed micro-computed tomography on skeletons of resident and migrant subspecies of the Dark-eyed Junco Junco hyemalis. We investigated the differences in the major wing bone, the humerus, and the major leg bone, the femur. In each bone, we studied the microarchitecture of the two types of bone tissue: cortical bone, the thick outer layer of bone; and trabecular bone, which is the porous network of bone tissue at the ends of long bones. We used linear models to quantify morphological features with respect to body mass and migratory behaviour. Humeri from migratory birds were thinner, wider and had higher overall geometric stiffness, i.e. a higher polar moment of inertia, relative to humeri from resident birds. These features may help keep their bones stiff to maintain their increased body mass during migration. In contrast, migrant femora were shorter, thinner and had lower geometric stiffness than femora of residents, potentially to reduce total body mass. Tissue mineral density was lower in both the humerus and the femur of migratory birds. In addition, migratory subspecies had less trabecular bone (lower bone volume fraction) due primarily to a loss of trabecular thickness. Migratory behaviour may thus select for improved stiffness and fatigue resistance in the wing bones and reduced mass of leg bones. Our work demonstrates how important insights into morphological adaptation can be obtained by investigating bone microstructure.     

An inventory of the possible effects of climatic change on western palearctic migratory birds

This paper presents an assessment of the possible effects of future climatic change on migratory birds. The assessment is based on two approaches: firstly an inventory is made of the environmental factors that may change which directly affect migratory birds. These factors include physical (temperature, hydrology, ocean and air streaming patterns) as well as biological (floral and faunal composition of ecosystems) and landuse aspects of the environment.Secondly, these possible changes were related to the annual cycles of migratory birds in order to estimate the problems that different groups of migratory birds have to cope with at various stages in their annual cycle. It is concluded that many migratory bird species will be influenced by climatic change, leading to adaptations in the birds annual cycle. The biggest problems may arise for those birds which depend on wetlands, because many of these wetlands may dessicate.     

北京野生水鸟迁徙规律及其监测策略初探

2005年全球暴发的禽流感疫情备受世界关注,候鸟带毒且野生水鸟是禽流感病毒的天然储库已被世界公认,我国野生动物疫源疫病监测工作已被提到重要议事日程.通过对2006～2008年监测数据的分析,发现北京市野生水鸟春季迁徙从2月下旬开始,4月初达到迁徙高峰;9月下旬开始秋季南迁,11月下旬达到迁徙高峰.并分别对北京地区雁鸭类、鹬鸻类、鹭类的迁徙规律进行了分析;根据北京的气候特点分析了野生水鸟的分布和迁徙特点;根据禽流感病毒与温度的关系,提出了北京的重点监测时期及物种.     

Daytime micro-naps in a nocturnal migrant: an EEG analysis

Many species of typically diurnal songbirds experience sleep loss during the migratory seasons owing to their nocturnal migrations. However, despite substantial loss of sleep, nocturnally migrating songbirds continue to function normally with no observable effect on their behaviour. It is unclear if and how avian migrants compensate for sleep loss. Recent behavioural evidence suggests that some species may compensate for lost night-time sleep with short, uni- and bilateral 'micro-naps' during the day. We provide electrophysiological evidence that short episodes of sleep-like daytime behaviour (approx. 12s) are accompanied by sleep-like changes in brain activity in an avian migrant. Furthermore, we present evidence that part of this physiological brain response manifests itself as unihemispheric sleep, a state during which one brain hemisphere is asleep while the other hemisphere remains essentially awake. Episodes of daytime sleep may represent a potent adaptation to the challenges of avian migration and offer a plausible explanation for the resilience to sleep loss in nocturnal migrants.     

Seasonally Changing Cryptochrome 1b Expression in the Retinal Ganglion Cells of a Migrating Passerine Bird

Cryptochromes, blue-light absorbing proteins involved in the circadian clock, have been proposed to be the receptor molecules of the avian magnetic compass. In birds, several cryptochromes occur: Cryptochrome 2, Cryptochrome 4 and two splice products of Cryptochrome 1, Cry1a and Cry1b. With an antibody not distinguishing between the two splice products, Cryptochrome 1 had been detected in the retinal ganglion cells of garden warblers during migration. A recent study located Cry1a in the outer segments of UV/V-cones in the retina of domestic chickens and European robins, another migratory species. Here we report the presence of cryptochrome 1b (eCry1b) in retinal ganglion cells and displaced ganglion cells of European Robins, Erithacus rubecula. Immuno-histochemistry at the light microscopic and electron microscopic level showed eCry1b in the cell plasma, free in the cytosol as well as bound to membranes. This is supported by immuno-blotting. However, this applies only to robins in the migratory state. After the end of the migratory phase, the amount of eCry1b was markedly reduced and hardly detectable. In robins, the amount of eCry1b in the retinal ganglion cells varies with season: it appears to be strongly expressed only during the migratory period when the birds show nocturnal migratory restlessness. Since the avian magnetic compass does not seem to be restricted to the migratory phase, this seasonal variation makes a role of eCry1b in magnetoreception rather unlikely. Rather, it could be involved in physiological processes controlling migratory restlessness and thus enabling birds to perform their nocturnal flights.     

Changes in migration phenology and biometrical traits of Reed,Marsh and Sedge Warblers

Global environmental processes like climate change could severely affect population level migratory behaviour of long range migrant birds. We analyzed changes in migration phenology and biometrics of three closely-related long-distance migrant Acrocephalus species. We used the records of 12 063 Sedge, 12 913 Reed, and 5 409 Marsh Warblers caught and ringed between 1989–2009, at a Hungarian stopover site. Quantile regressions were used to analyse the changes in spring and autumn migration phenology. Median spring arrival date of Sedge and Reed Warblers shifted 6.5 and 7.5 days earlier, respectively. Autumn arrival of all species shifted one (Reed and Marsh Warblers) or two (Sedge Warbler) weeks later. Mean body mass of adult Reed and Marsh Warblers decreased in spring (by 0.3 and 0.2 grams, respectively) and in autumn (by 0.8 and 0.2 grams, respectively) while body mass of adult Sedge Warblers decreased only in autumn (by 0.4 grams). Mean wing length of all species increased significantly (range of change: 0.6–1 mm). Despite the fact that the studied species are closely related, all three have remarkably different migration strategies. However, similar patterns can be observed in the studied parameters, indicating that global processes may have general effects on these species, albeit through markedly different mechanisms.     

Plasma corticosterone increases during migratory restlessness in the captive white-crowned sparrow Zonotrichia leucophrys gambelli

Plasma corticosterone increases during the period of spring migration in a variety of bird species. Long-distance migrants show elevations in corticosterone specifically in association with the stage of flight, suggesting that corticosterone may support flight-related processes, for example, locomotor activity and/or energy mobilization. The pattern of corticosterone secretion as it relates to migratory flight has hitherto not been clearly described in migrants that frequently interrupt flight to refuel, for example, the Gambel's white-crowned sparrow (Zonotrichia leucophrys gambelii). The Gambel's white-crowned sparrow fuels by day and expresses peak migratory activity during the first few hours of night. To determine if plasma corticosterone increases in association with the stage of migratory flight also in this short-bout migrant, we induced captive white-crowned sparrows to enter into the migratory condition by placing photosensitive birds on long days (16L:8D) and then evaluated birds for plasma corticosterone and locomotor activity during four time points of the day. Patterns found in long-day birds were compared to those observed in short-day controls (8L:16D). Differences in energy metabolism as determined from plasma metabolites were also evaluated. We found that locomotor activity and corticosterone were significantly elevated at the onset of the dark period, but only in long-day birds. Plasma beta-hydroxybutyrate (a ketone body) was also elevated. Thus, findings suggest that plasma corticosterone and ketogenesis increase in association with migratory restlessness in a short-bout migrant. In fact, corticosterone may play a regulatory role, because it shows a trend to increase already before night-time activity.