Migratory network reveals unique spatial-temporal migration dynamics of Dunlin subspecies along the East Asian-Australasian Flyway.

Determining the dynamics of where and when individuals occur is necessary to understand population declines and identify critical areas for populations of conservation concern. However, there are few examples where a spatially and temporally explicit model has been used to evaluate the migratory dynamics of a bird population across its entire annual cycle. We used geolocator-derived migration tracks of 84 Dunlin (Calidris alpina) on the East Asian-Australasian Flyway (EAAF) to construct a migratory network describing annual subspecies-specific migration patterns in space and time. We found that Dunlin subspecies exhibited unique patterns of spatial and temporal flyway use. Spatially, C. a. arcticola predominated in regions along the eastern edge of the flyway (e.g., western Alaska and central Japan), whereas C. a. sakhalina predominated in regions along the western edge of the flyway (e.g., N China and inland China). No individual Dunlin that wintered in Japan also wintered in the Yellow Sea, China seas, or inland China, and vice-versa. However, similar proportions of the 4 subspecies used many of the same regions at the center of the flyway (e.g., N Sakhalin Island and the Yellow Sea). Temporally, Dunlin subspecies staggered their south migrations and exhibited little temporal overlap among subspecies within shared migration regions. In contrast, Dunlin subspecies migrated simultaneously during north migration. South migration was also characterized by individuals stopping more often and for more days than during north migration. Taken together, these spatial-temporal migration dynamics indicate Dunlin subspecies may be differentially affected by regional habitat change and population declines according to where and when they occur. We suggest that the migration dynamics presented here are useful for guiding on-the-ground survey efforts to quantify subspecies' use of specific sites, and to estimate subspecies' population sizes and long-term trends. Such studies would significantly advance our understanding of Dunlin space-time dynamics and the coordination of Dunlin conservation actions across the EAAF.

Global flyway evolution in red knots Calidris canutus and genetic evidence for a Nearctic refugium.

Present-day ecology and population structure are the legacies of past climate and habitat perturbations, and this is particularly true for species that are widely distributed at high latitudes. The red knot, Calidris canutus, is an arctic-breeding, long-distance migratory shorebird with six recognized subspecies defined by differences in morphology, migration behavior, and annual cycle phenology, in a global distribution thought to have arisen just since the last glacial maximum (LGM). We used nextRAD sequencing of 10,881 single-nucleotide polymorphisms (SNPs) to assess the neutral genetic structure and phylogeographic history of 172 red knots representing all known global breeding populations. Using population genetics approaches, including model-based scenario-testing in an approximate Bayesian computation (ABC) framework, we infer that red knots derive from two main lineages that diverged ca. 34,000 years ago, and thus most probably persisted at the LGM in both Palearctic and Nearctic refugia, followed by at least two instances of secondary contact and admixture. Within two Beringian subspecies (C. c. roselaari and rogersi), we detected previously unknown genetic structure among sub-populations sharing a migratory flyway, reflecting additional complexity in the phylogeographic history of the region. Conversely, we found very weak genetic differentiation between two Nearctic populations (rufa and islandica) with clearly divergent migratory phenotypes and little or no apparent contact throughout the annual cycle. Together, these results suggest that relative gene flow among migratory populations reflects a complex interplay of historical, geographical, and ecological factors.

Mismatch-induced growth reductions in a clade of Arctic-breeding shorebirds are rarely mitigated by increasing temperatures.

In seasonal environments subject to climate change, organisms typically show phenological changes. As these changes are usually stronger in organisms at lower trophic levels than those at higher trophic levels, mismatches between consumers and their prey may occur during the consumers' reproduction period. While in some species a trophic mismatch induces reductions in offspring growth, this is not always the case. This variation may be caused by the relative strength of the mismatch, or by mitigating factors like increased temperature-reducing energetic costs. We investigated the response of chick growth rate to arthropod abundance and temperature for six populations of ecologically similar shorebirds breeding in the Arctic and sub-Arctic (four subspecies of Red Knot Calidris canutus, Great Knot C. tenuirostris and Surfbird C. virgata). In general, chicks experienced growth benefits (measured as a condition index) when hatching before the seasonal peak in arthropod abundance, and growth reductions when hatching after the peak. The moment in the season at which growth reductions occurred varied between populations, likely depending on whether food was limiting growth before or after the peak. Higher temperatures led to faster growth on average, but could only compensate for increasing trophic mismatch for the population experiencing the coldest conditions. We did not find changes in the timing of peaks in arthropod availability across the study years, possibly because our series of observations was relatively short; timing of hatching displayed no change over the years either. Our results suggest that a trend in trophic mismatches may not yet be evident; however, we show Arctic-breeding shorebirds to be vulnerable to this phenomenon and vulnerability to depend on seasonal prey dynamics.

Population genomics of two congeneric Palaearctic shorebirds reveals differential impacts of Quaternary climate oscillations across habitats types.

Intracontinental biotic divisions across the vast Palaearctic region are not well-characterized. Past research has revealed patterns ranging from a lack of population structure to deep divergences along varied lines of separation. Here we compared biogeographic patterns of two Palaearctic shorebirds with different habitat preferences, Whimbrel (Numenius phaeopus) and Eurasian curlew (N. arquata). Using genome-wide markers from populations across the Palaearctic, we applied a multitude of population genomic and phylogenomic approaches to elucidate population structure. Most importantly, we tested for isolation by distance and visualized barriers and corridors to gene flow. We found shallow Palaearctic population structure in subpolar bog and tundra-breeding whimbrels, consistent with other species breeding at a similarly high latitude, indicating connectivity across the tundra belt, both presently and during southward shifts in periods of global cooling. In contrast, the temperate grassland-breeding Eurasian curlew emerged in three distinct clades corresponding to glacial refugia. Barriers to gene flow coincided with areas of topographic relief in the central Palaearctic for whimbrels and further east for Eurasian curlews. Our findings highlight the interplay of historic and ecological factors in influencing present-day population structure of Palaearctic biota.

Response to Comment on "Global pattern of nest predation is disrupted by climate change in shorebirds".

Bulla et al dispute our main conclusion that the global pattern of nest predation is disrupted in shorebirds. We disagree with Bulla et al's conclusions and contest the robustness of their outcomes. We reaffirm our results that provide clear evidence that nest predation has increased significantly in shorebirds, especially in the Arctic.

Phylogenetic position of the presumably extinct slender-billed curlew, Numenius tenuirostris.

The high-capacity DNA analysis of museum samples opens new opportunities, associated with the investigation of extinct species evolution. Here, the complete mitochondrial genome of the presumably extinct bird species, the slender-billed curlew Numenius tenuirostris (Charadriiformes: Scolopacidae) is presented. Our results showed that mitochondrial DNA (mtDNA) is 16,705 base pairs (bp) in length and contain 13 protein-coding genes, two rRNA genes, and 22 tRNA genes. The overall base composition of the genome is 30.8% - A, 29.8% - C, 25.4% - T, 14.0% - G, and without a significant GC bias of 43.7%. Phylogenetic analyses based on the cytochrome B (cytB) gene and the whole mtDNA sequences revealed that N. tenuirostris had a close genetic relationship to Eurasian curlew (N. arquata), Far Eastern curlew (N. madagascariensis), and long-billed curlew - N. americanus. Besides, it reveals that Numenius genus is genetically distant from other Scolopacidae taxons. Together, these results provide a clear genetic perspective into the speciation process among the curlew genus members and points to a clear taxonomic position of N. tenuirostris.

Global pattern of nest predation is disrupted by climate change in shorebirds.

Ongoing climate change is thought to disrupt trophic relationships, with consequences for complex interspecific interactions, yet the effects of climate change on species interactions are poorly understood, and such effects have not been documented at a global scale. Using a single database of 38,191 nests from 237 populations, we found that shorebirds have experienced a worldwide increase in nest predation over the past 70 years. Historically, there existed a latitudinal gradient in nest predation, with the highest rates in the tropics; however, this pattern has been recently reversed in the Northern Hemisphere, most notably in the Arctic. This increased nest predation is consistent with climate-induced shifts in predator-prey relationships.

Intercontinental genetic structure and gene flow in Dunlin (Calidris alpina), a potential vector of avian influenza.

Waterfowl (Anseriformes) and shorebirds (Charadriiformes) are the most common wild vectors of influenza A viruses. Due to their migratory behavior, some may transmit disease over long distances. Migratory connectivity studies can link breeding and nonbreeding grounds while illustrating potential interactions among populations that may spread diseases. We investigated Dunlin (Calidris alpina), a shorebird with a subspecies (C. a. arcticola) that migrates from nonbreeding areas endemic to avian influenza in eastern Asia to breeding grounds in northern Alaska. Using microsatellites and mitochondrial DNA, we illustrate genetic structure among six subspecies: C. a. arcticola,C. a. pacifica,C. a. hudsonia,C. a. sakhalina,C. a. kistchinski, and C. a. actites. We demonstrate that mitochondrial DNA can help distinguish C. a. arcticola on the Asian nonbreeding grounds with >70% accuracy depending on their relative abundance, indicating that genetics can help determine whether C. a. arcticola occurs where they may be exposed to highly pathogenic avian influenza (HPAI) during outbreaks. Our data reveal asymmetric intercontinental gene flow, with some C. a. arcticola short-stopping migration to breed with C. a. pacifica in western Alaska. Because C. a. pacifica migrates along the Pacific Coast of North America, interactions between these subspecies and other taxa provide route for transmission of HPAI into other parts of North America.

Flexibility and constraints in the molt schedule of long-distance migratory shorebirds: causes and consequences.

Molt is a major component of the annual cycle of birds, the timing and extent of which can affect body condition, survival, and future reproductive success through carry-over effects. The way in which molt is fitted into the annual cycle seems to be a somewhat neglected area which is both of interest and of importance. Study of the causes of annual variation in the timing of molt and its potential consequence in long-distance migratory birds was examined using the Curlew Sandpiper, Calidris ferruginea, as a model species. Using the maximum likelihood molt models of Underhill and Zucchini (1988, Ibis 130:358-372), the relationship between annual variability in the start dates of molt at the population level with conditions on the breeding area was explored. Adult males typically started early in years when temperature in June on the Arctic breeding grounds were high compared to cold years while adult females molted later in years of high breeding success and/or warm July temperature and vice versa. When molt started later, the duration was often shorter, indicating that late completion of molt might have fitness consequences, probably jeopardizing survival. Evidence of this was seen in the low body condition of birds in years when molt was completed late. The results indicate that these migratory shorebirds follow a fine-tuned annual life cycle, and disturbances at a certain stage can alter next biological events through carry-over effects.