Migratory birds modulate niche tradeoffs in rhythm with seasons and life history.

Movement is a key means by which animals cope with variable environments. As they move, animals construct individual niches composed of the environmental conditions they experience. Niche axes may vary over time and covary with one another as animals make tradeoffs between competing needs. Seasonal migration is expected to produce substantial niche variation as animals move to keep pace with major life history phases and fluctuations in environmental conditions. Here, we apply a time-ordered principal component analysis to examine dynamic niche variance and covariance across the annual cycle for four species of migratory crane: common crane (Grus grus, n = 20), demoiselle crane (Anthropoides virgo, n = 66), black-necked crane (Grus nigricollis, n = 9), and white-naped crane (Grus vipio, n = 9). We consider four key niche components known to be important to aspects of crane natural history: enhanced vegetation index (resources availability), temperature (thermoregulation), crop proportion (preferred foraging habitat), and proximity to water (predator avoidance). All species showed a primary seasonal niche "rhythm" that dominated variance in niche components across the annual cycle. Secondary rhythms were linked to major species-specific life history phases (migration, breeding, and nonbreeding) as well as seasonal environmental patterns. Furthermore, we found that cranes' experiences of the environment emerge from time-dynamic tradeoffs among niche components. We suggest that our approach to estimating the environmental niche as a multidimensional and time-dynamical system of tradeoffs improves mechanistic understanding of organism-environment interactions.

Ixodid ticks from wild and domestic animals in East and Central Asian flyways.

Tick-borne diseases have a significant impact on human and animal populations, posing an increasing threat to public health, particularly in the context of climate change. Along with the various natural hosts of ticks, birds play a notable role in transmitting ticks and tick-borne pathogens, indicating the importance of monitoring flyways and establishing a cooperative network for comprehensive surveillance and to collect diverse tick samples across various regions. This study aimed to develop an international network for surveillance of disease, collection of sufficient tick samples, and overall identification of the geographical distribution of host and ticks in Asian regions, especially in 11 countries on East Asian and Central Asian flyways. Ticks were collected from wild animals, domestic animals, and vegetation to identify the differences between Ixodid ticks and understand tick distribution. We collected a total 6,624 of ticks from 11 collaborating Asian countries, the Republic of Korea (ROK), Japan, Thailand, Philippines, Indonesia, Cambodia, Vietnam, Taiwan, Hong Kong, Mongolia and Pakistan. We identified 17 host animals and 47 species of both residential and migratory birds. Ticks from birds collected from four countries (ROK, Japan, Hong Kong and Mongolia) belonged to two genera, Haemaphysalis and Ixodes, including Haemaphysalis (H.) longicornis, H. flava, H. concinna, H. hystricis, H. formosensis, Ixodes (I.) nipponensis and I. persulcatus. The potential of migratory birds to cross ecological barriers with ticks and tick-borne diseases indicated the need for further investigations to understand the migration of birds as potential vectors and the new influx of zoonotic diseases along migratory bird flyways. This study suggests the potential risk of spreading tick-borne diseases through birds, thus highlighting the importance of international cooperative networking.

Breeding and migration performance metrics highlight challenges for White-naped Cranes.

Globally, habitat loss has been deemed a major threat to wetland bird populations. However, the underlying mechanism of population declines and variations in the birds' vulnerability throughout their annual cycle is challenging to determine, yet critical for development of targeted conservation strategies. Over seven years, landscape water availability explained occupancy of breeding territories best when breeding performance, migratory performance, and annual survival of the White-naped Crane (Grus vipio) population in eastern Mongolia were studied. Also, the hatching success of eggs was positively correlated with water availability in addition to plant productivity. High ambient temperatures and large numbers of herder families (and hence more livestock) negatively affected hatching success. High water availability at Luan, a major stopover site increased migration speed during the cranes' northbound migration to their breeding grounds. In contrast, when water conditions were favorable, the birds stayed longer at the stopover site during southbound migration. Increased human density reduced the use of the stopover site during northbound migration. Finally, cranes arrived early at the breeding grounds when ambient temperature was high in northeast Mongolia. Combining these findings with historical trends in key environmental factors on their breeding grounds explains the general decline observed in this population of cranes in recent decades. Extrapolating our findings with future climate predictions, the outlook seems poor unless urgent action is taken. Knowledge of the mechanisms underlying White-naped Crane population decline in eastern Mongolia identified in this paper should improve the effectiveness of these actions.

Arctic introgression and chromatin regulation facilitated rapid Qinghai-Tibet Plateau colonization by an avian predator.

The Qinghai-Tibet Plateau (QTP), possesses a climate as cold as that of the Arctic, and also presents uniquely low oxygen concentrations and intense ultraviolet (UV) radiation. QTP animals have adapted to these extreme conditions, but whether they obtained genetic variations from the Arctic during cold adaptation, and how genomic mutations in non-coding regions regulate gene expression under hypoxia and intense UV environment, remain largely unknown. Here, we assemble a high-quality saker falcon genome and resequence populations across Eurasia. We identify female-biased hybridization with Arctic gyrfalcons in the last glacial maximum, that endowed eastern sakers with alleles conveying larger body size and changes in fat metabolism, predisposing their QTP cold adaptation. We discover that QTP hypoxia and UV adaptations mainly involve independent changes in non-coding genomic variants. Our study highlights key roles of gene flow from Arctic relatives during QTP hypothermia adaptation, and cis-regulatory elements during hypoxic response and UV protection.

Differences in on-ground and aloft conditions explain seasonally different migration paths in Demoiselle crane.

BACKGROUND: Although some migratory birds may take different routes during their outbound and inbound migration, the factors causing these differential migrations to and from the breeding grounds, have rarely been investigated. In Northeast Asia, Demoiselle crane (Anthropoides virgo) performs one of the most extreme "loop" migrations known to date. During outbound migration, they cross the Himalayas to non-breeding sites in northwest India. Contrastingly, during inbound migration to the breeding grounds, they fly around the western end of the Himalayas. We hypothesise that differences in prevailing environmental conditions aloft and/or on-ground during both seasonal migrations are at the core of this phenomenon. METHODS: Based on the tracking data of 16 individuals of tagged Demoiselle crane, we compared conditions during actual migration with those of simulated "reverse" migration (i.e. by adding 180 degrees to the flight direction and adding and subtracting half a year to the timestamps of outbound and inbound migration, respectively). RESULTS: The comparison of actual and simulated "reverse" migration indicated that cranes would have encountered poorer aloft (wind support and thermal uplift) and on-ground conditions (temperature) if they had migrated in a reverse outbound migration and poorer on-ground conditions (Normalised Difference Vegetation Indexes [NDVI]) if they had migrated in a reverse inbound direction. CONCLUSIONS: Our analyses suggest that both on-ground and aloft conditions play a key role in explaining Demoiselle cranes' loop migration, during the periods that they chose to use these alternative routes. Knowledge on the determinants of (differential) migration routes allow predicting migration decisions and may be critical in mitigating global change effects on animal migrations.

Range-wide breeding habitat use of the critically endangered Yellow-breasted Bunting Emberiza aureola after population collapse.

The population of the Yellow-breasted Bunting Emberiza aureola, a formerly widely distributed and abundant songbird of northern Eurasia, suffered a catastrophic decline and a strong range contraction between 1980 and 2013. There is evidence that the decline was driven by illegal trapping during migration, but potential contributions of other factors to the decline, such as land-use change, have not yet been evaluated. Before the effects of land-use change can be evaluated, a basic understanding of the ecological requirements of the species is needed. We therefore compared habitat use in ten remaining breeding regions across the range, from European Russia to Japan and the Russian Far East. We also assessed large-scale variation in habitat parameters across the breeding range. We found large variation in habitat use, within and between populations. Differences were related to the cover and height of trees and shrubs at Yellow-breasted Bunting territories. In many regions, Yellow-breasted Buntings occupied early successional stages, including anthropogenic habitats characterized by mowing, grazing, or fire regimes. We found that the probability of presence can be best predicted with the cover of shrubs, herbs, and grasses. Highest probabilities were found at shrub cover values of 40%-70%. Differences in habitat use along a longitudinal gradient were small, but we found strong differences across latitudes, possibly related to habitat availability. We conclude that the remaining Yellow-breasted Bunting populations are not limited to specific habitat types. Our results provide important baseline information to model the range-wide distribution of this critically endangered species and to guide targeted conservation measures.

Lack of conspicuous sex-biased dispersal patterns at different spatial scales in an Asian endemic goose species breeding in unpredictable steppe wetlands.

Dispersal affects the spatial distribution and population structure of species. Dispersal is often male-biased in mammals while female-biased in birds, with the notable exception of the Anatidae. In this study, we tested genetic evidence for sex-biased dispersal (SBD) in the Swan Goose Anser cygnoides, an Asian endemic and IUCN vulnerable species, which has been increasingly restricted to breeding on Mongolian steppe wetlands. We analyzed the genotypes of 278 Swan Geese samples from 14 locations at 14 microsatellite loci. Results from assignment indices, analysis of molecular variance, and five other population descriptors all failed to support significant SBD signals for the Swan Goose at the landscape level. Although overall results showed significantly high relatedness within colonies (suggesting high levels of philopatry in both sexes), local male genetic structure at the 1,050 km distance indicated greater dispersal distance for females from the eastern sector of the breeding range. Hence, local dispersal is likely scale-dependent and female-biased within the eastern breeding range. These findings are intriguing considering the prevailing expectation for there to be female fidelity in most goose species. We suggest that while behavior-related traits may have facilitated the local genetic structure for the Swan Goose, several extrinsic factors, including the decreasing availability of the nesting sites and the severe fragmentation of breeding habitats, could have contributed to the absence of SBD at the landscape level. The long-distance molt migration that is typical of goose species such as the Swan Goose may also have hampered our ability to detect SBD. Hence, we urge further genetic sampling from other areas in summer to extend our results, complemented by field observations to confirm our DNA analysis conclusions about sex-specific dispersal patterns at different spatial scales in this species.

Consistent habitat preference underpins the geographically divergent autumn migration of individual Mongolian common shelducks.

While many avian populations follow narrow, well-defined "migratory corridors," individuals from other populations undertake highly divergent individual migration routes, using widely dispersed stopover sites en route between breeding and wintering areas, although the reasons for these differences are rarely investigated. We combined individual GPS-tracked migration data from Mongolian-breeding common shelduck Tadorna tadorna and remote sensing datasets, to investigate habitat selection at inland stopover sites used by these birds during dispersed autumn migration, to explain their divergent migration patterns. We used generalized linear mixed models to investigate population-level resource selection, and generalized linear models to investigate stopover-site-level resource selection. The population-level model showed that water recurrence had the strongest positive effect on determining birds' occupancy at staging sites, while cultivated land and grassland land cover type had strongest negative effects; effects of other land cover types were negative but weaker, particularly effects of water seasonality and presence of a human footprint, which were positive but weak or non-significant, respectively. Although stopover-site-level models showed variable resource selection patterns, the variance partitioning and cross-prediction AUC scores corroborated high inter-individual consistency in habitat selection at inland stopover sites during the dispersed autumn migration. These results suggest that the geographically widespread distribution (and generally rarity) of suitable habitats explained the spatially divergent autumn migrations of Mongolian breeding common shelduck, rather than the species showing flexible autumn staging habitat occupancy.

Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome.

Disease outbreaks and pathogen introductions can have significant effects on host populations, and the ability of pathogens to persist in the environment can exacerbate disease impacts by fueling sustained transmission, seasonal epidemics, and repeated spillover events. While theory suggests that the presence of an environmental reservoir increases the risk of host declines and threat of extinction, the influence of reservoir dynamics on transmission and population impacts remains poorly described. Here we show that the extent of the environmental reservoir explains broad patterns of host infection and the severity of disease impacts of a virulent pathogen. We examined reservoir and host infection dynamics and the resulting impacts of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome, in 39 species of bats at 101 sites across the globe. Lower levels of pathogen in the environment consistently corresponded to delayed infection of hosts, fewer and less severe infections, and reduced population impacts. In contrast, an extensive and persistent environmental reservoir led to early and widespread infections and severe population declines. These results suggest that continental differences in the persistence or decay of P. destructans in the environment altered infection patterns in bats and influenced whether host populations were stable or experienced severe declines from this disease. Quantifying the impact of the environmental reservoir on disease dynamics can provide specific targets for reducing pathogen levels in the environment to prevent or control future epidemics.

Annual migratory patterns of Far East Greylag Geese (Anser anser rubrirostris) revealed by GPS tracking.

Twenty Far East Greylag Geese, Anser anser rubrirostris, were captured and fitted with Global Positioning System/Global System for Mobile Communications (GPS/GSM) loggers to identify breeding and wintering areas, migration routes and stopover sites. Telemetry data for the first time showed linkages between their Yangtze River wintering areas, stopover sites in northeastern China, and breeding/molting grounds in eastern Mongolia and northeast China. 10 of the 20 tagged individuals provided sufficient data. They stopped on migration at the Yellow River Estuary, Beidagang Reservoir and Xar Moron River, confirming these areas as being important stopover sites for this population. The median spring migration duration was 33.7 days (individuals started migrating between 25 February and 16 March and completed migrating from 1 to 9 April) compared to 52.7 days in autumn (26 September-13 October until 4 November-11 December). The median stopover duration was 31.1 and 51.3 days and the median speed of travel was 62.6 and 47.9 km/day for spring and autumn migration, respectively. The significant differences between spring and autumn migration on the migration duration, the stopover duration and the migration speed confirmed that tagged adult Greylag Geese traveled faster in spring than autumn, supporting the hypothesis that they should be more time-limited during spring migration.

Tackling the Tibetan Plateau in a down suit: insights into thermoregulation by bar-headed geese during migration.

Birds migrating through extreme environments can experience a range of challenges while meeting the demands of flight, including highly variable ambient temperatures, humidity and oxygen levels. However, there has been limited research into avian thermoregulation during migration in extreme environments. This study aimed to investigate the effect of flight performance and high altitude on body temperature (Tb) of free-flying bar-headed geese (Anser indicus), a species that completes a high-altitude trans-Himalayan migration through very cold, hypoxic environments. We measured abdominal Tb, along with altitude (via changes in barometric pressure), heart rate and body acceleration of bar-headed geese during their migration across the Tibetan Plateau. Bar-headed geese vary the circadian rhythm of Tb in response to migration, with peak daily Tb during daytime hours outside of migration but early in the morning or overnight during migration, reflecting changes in body acceleration. However, during flight, changes in Tb were not consistent with changes in flight performance (as measured by heart rate or rate of ascent) or altitude. Overall, our results suggest that bar-headed geese are able to thermoregulate during high-altitude migration, maintaining Tb within a relatively narrow range despite appreciable variation in flight intensity and environmental conditions.

Author Correction: Stochastic simulations reveal few green wave surfing populations among spring migrating herbivorous waterfowl.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Stochastic simulations reveal few green wave surfing populations among spring migrating herbivorous waterfowl.

Tracking seasonally changing resources is regarded as a widespread proximate mechanism underpinning animal migration. Migrating herbivores, for example, are hypothesized to track seasonal foliage dynamics over large spatial scales. Previous investigations of this green wave hypothesis involved few species and limited geographical extent, and used conventional correlation that cannot disentangle alternative correlated effects. Here, we introduce stochastic simulations to test this hypothesis using 222 individual spring migration episodes of 14 populations of ten species of geese, swans and dabbling ducks throughout Europe, East Asia, and North America. We find that the green wave cannot be considered a ubiquitous driver of herbivorous waterfowl spring migration, as it explains observed migration patterns of only a few grazing populations in specific regions. We suggest that ecological barriers and particularly human disturbance likely constrain the capacity of herbivorous waterfowl to track the green wave in some regions, highlighting key challenges in conserving migratory birds.

Mitochondrial Divergence between Western and Eastern Great Bustards: Implications for Conservation and Species Status.

The great bustard is the heaviest bird capable of flight and an iconic species of the Eurasian steppe. Populations of both currently recognized subspecies are highly fragmented and critically small in Asia. We used DNA sequence data from the mitochondrial cytochrome b gene and the mitochondrial control region to estimate the degree of mitochondrial differentiation and rates of female gene flow between the subspecies. We obtained genetic samples from 51 individuals of Otis tarda dybowskii representing multiple populations, including the first samples from Kazakhstan and Mongolia and samples from near the Altai Mountains, the proposed geographic divide between the subspecies, allowing for better characterization of the boundary between the 2 subspecies. We compared these with existing sequence data (n = 66) from Otis tarda tarda. Our results suggest, though do not conclusively prove, that O. t. dybowskii and O. t. tarda may be distinct species. The geographic distribution of haplotypes, phylogenetic analysis, analyses of molecular variance, and coalescent estimation of divergence time and female migration rates indicate that O. t. tarda and O. t. dybowskii are highly differentiated in the mitochondrial genome, have been isolated for approximately 1.4 million years, and exchange much less than 1 female migrant per generation. Our findings indicate that the 2 forms should at least be recognized and managed as separate evolutionary units. Populations in Xinjiang, China and Khövsgöl and Bulgan, Mongolia exhibited the highest levels of genetic diversity and should be prioritized in conservation planning.

Do Bar-Headed Geese Train for High Altitude Flights?

SYNOPSIS: Exercise at high altitude is extremely challenging, largely due to hypobaric hypoxia (low oxygen levels brought about by low air pressure). In humans, the maximal rate of oxygen consumption decreases with increasing altitude, supporting progressively poorer performance. Bar-headed geese (Anser indicus) are renowned high altitude migrants and, although they appear to minimize altitude during migration where possible, they must fly over the Tibetan Plateau (mean altitude 4800 m) for much of their annual migration. This requires considerable cardiovascular effort, but no study has assessed the extent to which bar-headed geese may train prior to migration for long distances, or for high altitudes. Using implanted loggers that recorded heart rate, acceleration, pressure, and temperature, we found no evidence of training for migration in bar-headed geese. Geese showed no significant change in summed activity per day or maximal activity per day. There was also no significant change in maximum heart rate per day or minimum resting heart rate, which may be evidence of an increase in cardiac stroke volume if all other variables were to remain the same. We discuss the strategies used by bar-headed geese in the context of training undertaken by human mountaineers when preparing for high altitude, noting the differences between their respective cardiovascular physiology.

Chewing Lice of Swan Geese (Anser cygnoides): New Host-Parasite Associations.

Chewing lice (Phthiraptera) that parasitize the globally threatened swan goose Anser cygnoides have been long recognized since the early 19th century, but those records were probably biased towards sampling of captive or domestic geese due to the small population size and limited distribution of its wild hosts. To better understand the lice species parasitizing swan geese that are endemic to East Asia, we collected chewing lice from 14 wild geese caught at 3 lakes in northeastern Mongolia. The lice were morphologically identified as 16 Trinoton anserinum (Fabricius, 1805), 11 Ornithobius domesticus Arnold, 2005, and 1 Anaticola anseris (Linnaeus, 1758). These species are known from other geese and swans, but all of them were new to the swan goose. This result also indicates no overlap in lice species between older records and our findings from wild birds. Thus, ectoparasites collected from domestic or captive animals may provide biased information on the occurrence, prevalence, host selection, and host-ectoparasite interactions from those on wild hosts.

A new method for discovering behavior patterns among animal movements.

Advanced satellite tracking technologies enable biologists to track animal movements at fine spatial and temporal scales. The resultant data present opportunities and challenges for understanding animal behavioral mechanisms. In this paper, we develop a new method to elucidate animal movement patterns from tracking data. Here, we propose the notion of continuous behavior patterns as a concise representation of popular migration routes and underlying sequential behaviors during migration. Each stage in the pattern is characterized in terms of space (i.e., the places traversed during movements) and time (i.e. the time spent in those places); that is, the behavioral state corresponding to a stage is inferred according to the spatiotemporal and sequential context. Hence, the pattern may be interpreted predictably. We develop a candidate generation and refinement framework to derive all continuous behavior patterns from raw trajectories. In the framework, we first define the representative spots to denote the underlying potential behavioral states that are extracted from individual trajectories according to the similarity of relaxed continuous locations in certain distinct time intervals. We determine the common behaviors of multiple individuals according to the spatiotemporal proximity of representative spots and apply a projection-based extension approach to generate candidate sequential behavior sequences as candidate patterns. Finally, the candidate generation procedure is combined with a refinement procedure to derive continuous behavior patterns. We apply an ordered processing strategy to accelerate candidate refinement. The proposed patterns and discovery framework are evaluated through conceptual experiments on both real GPS-tracking and large synthetic datasets.

Mapping migratory flyways in Asia using dynamic Brownian bridge movement models.

BACKGROUND: Identifying movement routes and stopover sites is necessary for developing effective management and conservation strategies for migratory animals. In the case of migratory birds, a collection of migration routes, known as a flyway, is often hundreds to thousands of kilometers long and can extend across political boundaries. Flyways encompass the entire geographic range between the breeding and non-breeding areas of a population, species, or a group of species, and they provide spatial frameworks for management and conservation across international borders. Existing flyway maps are largely qualitative accounts based on band returns and survey data rather than observed movement routes. In this study, we use satellite and GPS telemetry data and dynamic Brownian bridge movement models to build upon existing maps and describe waterfowl space use probabilistically in the Central Asian and East Asian-Australasian Flyways. RESULTS: Our approach provided new information on migratory routes that was not easily attainable with existing methods to describe flyways. Utilization distributions from dynamic Brownian bridge movement models identified key staging and stopover sites, migration corridors and general flyway outlines in the Central Asian and East Asian-Australasian Flyways. A map of space use from ruddy shelducks depicted two separate movement corridors within the Central Asian Flyway, likely representing two distinct populations that show relatively strong connectivity between breeding and wintering areas. Bar-headed geese marked at seven locations in the Central Asian Flyway showed heaviest use at several stopover sites in the same general region of high-elevation lakes along the eastern Qinghai-Tibetan Plateau. Our analysis of data from multiple Anatidae species marked at sites throughout Asia highlighted major movement corridors across species and confirmed that the Central Asian and East Asian-Australasian Flyways were spatially distinct. CONCLUSIONS: The dynamic Brownian bridge movement model improves our understanding of flyways by estimating relative use of regions in the flyway while providing detailed, quantitative information on migration timing and population connectivity including uncertainty between locations. This model effectively quantifies the relative importance of different migration corridors and stopover sites and may help prioritize specific areas in flyways for conservation of waterbird populations.