Arriving late and lean at a stopover site is selected against in a declining migratory bird population.

Loss and/or deterioration of refuelling habitats have caused population declines in many migratory bird species but whether this results from unequal mortality among individuals varying in migration traits remains to be shown. Based on 13 years of body mass and size data of great knots (Calidris tenuirostris) at a stopover site of the Yellow Sea, combined with resightings of individuals marked at this stopover site along the East Asian-Australasian Flyway, we assessed year to year changes in annual apparent survival rates, and how apparent survival differed between migration phenotypes (i.e. migration timing and fuel stores). The measurements occurred over a period of habitat loss and/or deterioration in this flyway. We found that the annual apparent survival rates of great knots rapidly declined from 2006 to 2018, late-arriving individuals with small fuel stores exhibiting the lowest apparent survival rate. There was an advancement in mean arrival date and an increase in the mean fuel load of stopping birds over the study period. Our results suggest that late-arriving individuals with small fuel loads were selected against. Thus, habitat loss and/or deterioration at staging sites may cause changes in the composition of migratory phenotypes at the population-level.

Migration strategy as an indicator of resilience to change in two shorebird species with contrasting population trajectories.

Many migratory birds are declining worldwide. In line with the general causes for the global biodiversity crisis, habitat loss, pollution, hunting, over-exploitation and climate change are thought to be at the basis of these population declines. Long-distance migrants seem especially vulnerable to rapid anthropogenic change, yet, the rate of decline across populations and species varies greatly within flyways. We hypothesize that differences in migration strategy, and notably stopover-site use, may be at the basis of these variations in resilience to global change. By identifying and comparing the migration strategies of two very closely related shorebird species, the Curlew sandpiper Calidris ferruginea and the Red-necked stint Calidris ruficollis, migrating from the same non-breeding site in Australia to similar breeding sites in the high Russian Arctic, we aimed to explain why these two species express differential resilience to rapid changes within their flyway resulting in different population trajectories in recent times. Based on 13 Curlew sandpiper and 16 Red-necked stint tracks from light-level geolocator tags, we found that individual Curlew sandpipers make use of fewer stopover areas along the flyway compared to Red-necked stints. Furthermore, and notably during northward migration, Curlew sandpipers have a higher dependency on fewer sites, both in terms of the percentage of individuals visiting key stopover sites and the relative time spent at those sites. While Curlew sandpipers rely mainly on the Yellow Sea region, which has recently experienced a sharp decline in suitable habitat, Red-necked stints make use of additional sites and spread their relative time en-route across sites more evenly. Our results indicate that differential migration strategies may explain why Curlew sandpipers within the East Asian-Australasian Flyway are declining rapidly (9.5%-5.5% per year) while Red-necked stints remain relatively stable (-3.1%-0%). We consider that more generally, the number of sites per individual and among a population, the spatial distribution across the flyway, as well as the relationship between the time spent over sites may prove to be key variables explaining populations and species' differential resilience to environmental change.

Influenza A Viruses in Ruddy Turnstones (Arenaria interpres); Connecting Wintering and Migratory Sites with an Ecological Hotspot at Delaware Bay.

Each May for over three decades, avian influenza A viruses (IAVs) have been isolated from shorebirds and gulls (order Charadriiformes) at Delaware Bay (DE Bay), USA, which is a critical stopover site for shorebirds on their spring migration to arctic breeding grounds. At DE Bay, most isolates have been recovered from ruddy turnstones (Arenaria interpres), but it is unknown if this species is involved in either the maintenance or movement of these viruses outside of this site. We collected and tested fecal samples from 2823 ruddy turnstones in Florida and Georgia in the southeastern United States during four winter/spring sample periods-2010, 2011, 2012, and 2013-and during the winters of 2014/2015 and 2015/2016. Twenty-five low pathogenicity IAVs were recovered representing five subtypes (H3N4, H3N8, H5N9, H6N1, and H12N2). Many of these subtypes matched those recovered at DE Bay during the previous year or that year's migratory cycle, suggesting that IAVs present on these southern wintering areas represent a source of virus introduction to DE Bay via migrating ruddy turnstones. Analyses of all IAV gene segments of H5N9 and H6N1 viruses recovered from ruddy turnstones at DE Bay during May 2012 and from the southeast during the spring of 2012 revealed a high level of genetic relatedness at the nucleotide level, suggesting that migrating ruddy turnstones move IAVs from wintering grounds to the DE Bay ecosystem.

Time versus energy minimization migration strategy varies with body size and season in long-distance migratory shorebirds.

BACKGROUND: Migrants have been hypothesised to use different migration strategies between seasons: a time-minimization strategy during their pre-breeding migration towards the breeding grounds and an energy-minimization strategy during their post-breeding migration towards the wintering grounds. Besides season, we propose body size as a key factor in shaping migratory behaviour. Specifically, given that body size is expected to correlate negatively with maximum migration speed and that large birds tend to use more time to complete their annual life-history events (such as moult, breeding and migration), we hypothesise that large-sized species are time stressed all year round. Consequently, large birds are not only likely to adopt a time-minimization strategy during pre-breeding migration, but also during post-breeding migration, to guarantee a timely arrival at both the non-breeding (i.e. wintering) and breeding grounds. METHODS: We tested this idea using individual tracks across six long-distance migratory shorebird species (family Scolopacidae) along the East Asian-Australasian Flyway varying in size from 50 g to 750 g lean body mass. Migration performance was compared between pre- and post-breeding migration using four quantifiable migratory behaviours that serve to distinguish between a time- and energy-minimization strategy, including migration speed, number of staging sites, total migration distance and step length from one site to the next. RESULTS: During pre- and post-breeding migration, the shorebirds generally covered similar distances, but they tended to migrate faster, used fewer staging sites, and tended to use longer step lengths during pre-breeding migration. These seasonal differences are consistent with the prediction that a time-minimization strategy is used during pre-breeding migration, whereas an energy-minimization strategy is used during post-breeding migration. However, there was also a tendency for the seasonal difference in migration speed to progressively disappear with an increase in body size, supporting our hypothesis that larger species tend to use time-minimization strategies during both pre- and post-breeding migration. CONCLUSIONS: Our study highlights that body size plays an important role in shaping migratory behaviour. Larger migratory bird species are potentially time constrained during not only the pre- but also the post-breeding migration. Conservation of their habitats during both seasons may thus be crucial for averting further population declines.

Rapid population decline in migratory shorebirds relying on Yellow Sea tidal mudflats as stopover sites.

Migratory animals are threatened by human-induced global change. However, little is known about how stopover habitat, essential for refuelling during migration, affects the population dynamics of migratory species. Using 20 years of continent-wide citizen science data, we assess population trends of ten shorebird taxa that refuel on Yellow Sea tidal mudflats, a threatened ecosystem that has shrunk by >65% in recent decades. Seven of the taxa declined at rates of up to 8% per year. Taxa with the greatest reliance on the Yellow Sea as a stopover site showed the greatest declines, whereas those that stop primarily in other regions had slowly declining or stable populations. Decline rate was unaffected by shared evolutionary history among taxa and was not predicted by migration distance, breeding range size, non-breeding location, generation time or body size. These results suggest that changes in stopover habitat can severely limit migratory populations.

Unexpected diversity in socially synchronized rhythms of shorebirds.

The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions, but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators. Individuals can temporally segregate their daily activities (for example, prey avoiding predators, subordinates avoiding dominants) or synchronize their activities (for example, group foraging, communal defence, pairs reproducing or caring for offspring). The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood. Here we investigate these rhythms in the context of biparental care, a particularly sensitive phase of social synchronization where pair members potentially compromise their individual rhythms. Using data from 729 nests of 91 populations of 32 biparentally incubating shorebird species, where parents synchronize to achieve continuous coverage of developing eggs, we report remarkable within- and between-species diversity in incubation rhythms. Between species, the median length of one parent's incubation bout varied from 1-19 h, whereas period length-the time in which a parent's probability to incubate cycles once between its highest and lowest value-varied from 6-43 h. The length of incubation bouts was unrelated to variables reflecting energetic demands, but species relying on crypsis (the ability to avoid detection by other animals) had longer incubation bouts than those that are readily visible or who actively protect their nest against predators. Rhythms entrainable to the 24-h light-dark cycle were less prevalent at high latitudes and absent in 18 species. Our results indicate that even under similar environmental conditions and despite 24-h environmental cues, social synchronization can generate far more diverse behavioural rhythms than expected from studies of individuals in captivity. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms.

Why fly the extra mile? Latitudinal trend in migratory fuel deposition rate as driver of trans-equatorial long-distance migration.

Trans-equatorial long-distance migrations of high-latitude breeding animals have been attributed to narrow ecological niche widths. We suggest an alternative hypothesis postulating that trans-equatorial migrations result from a possible increase in the rate at which body stores to fuel migration are deposited with absolute latitude; that is, longer, migrations away from the breeding grounds surpassing the equator may actually enhance fueling rates on the nonbreeding grounds and therewith the chance of a successful, speedy and timely migration back to the breeding grounds. To this end, we first sought to confirm the existence of a latitudinal trend in fuel deposition rate in a global data set of free-living migratory shorebirds and investigated the potential factors causing this trend. We next tested two predictions on how this trend is expected to impact the migratory itineraries on northward migration under the time-minimization hypothesis, using 56 tracks of high-latitude breeding shorebirds migrating along the East Asian-Australasian Flyway. We found a strong positive effect of latitude on fuel deposition rate, which most likely relates to latitudinal variations in primary productivity and available daily foraging time. We next confirmed the resulting predictions that (1) when flying from a stopover site toward the equator, migrants use long jumps that will take them to an equivalent or higher latitude at the opposite hemisphere; and (2) that from here onward, migrants will use small steps, basically fueling only enough to make it to the next suitable staging site. These findings may explain why migrants migrate "the extra mile" across the equator during the nonbreeding season in search of better fueling conditions, ultimately providing secure and fast return migrations to the breeding grounds in the opposite hemisphere.

Effects of geolocators on hatching success, return rates, breeding movements, and change in body mass in 16 species of Arctic-breeding shorebirds.

BACKGROUND: Geolocators are useful for tracking movements of long-distance migrants, but potential negative effects on birds have not been well studied. We tested for effects of geolocators (0.8-2.0 g total, representing 0.1-3.9 % of mean body mass) on 16 species of migratory shorebirds, including five species with 2-4 subspecies each for a total of 23 study taxa. Study species spanned a range of body sizes (26-1091 g) and eight genera, and were tagged at 23 breeding and eight nonbreeding sites. We compared breeding performance and return rates of birds with geolocators to control groups while controlling for potential confounding variables. RESULTS: We detected negative effects of tags for three small-bodied species. Geolocators reduced annual return rates for two of 23 taxa: by 63 % for semipalmated sandpipers and by 43 % for the arcticola subspecies of dunlin. High resighting effort for geolocator birds could have masked additional negative effects. Geolocators were more likely to negatively affect return rates if the total mass of geolocators and color markers was 2.5-5.8 % of body mass than if tags were 0.3-2.3 % of body mass. Carrying a geolocator reduced nest success by 42 % for semipalmated sandpipers and tripled the probability of partial clutch failure in semipalmated and western sandpipers. Geolocators mounted perpendicular to the leg on a flag had stronger negative effects on nest success than geolocators mounted parallel to the leg on a band. However, parallel-band geolocators were more likely to reduce return rates and cause injuries to the leg. No effects of geolocators were found on breeding movements or changes in body mass. Among-site variation in geolocator effect size was high, suggesting that local factors were important. CONCLUSIONS: Negative effects of geolocators occurred only for three of the smallest species in our dataset, but were substantial when present. Future studies could mitigate impacts of tags by reducing protruding parts and minimizing use of additional markers. Investigators could maximize recovery of tags by strategically deploying geolocators on males, previously marked individuals, and successful breeders, though targeting subsets of a population could bias the resulting migratory movement data in some species.

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.

Migratory connectivity magnifies the consequences of habitat loss from sea-level rise for shorebird populations.

Sea-level rise (SLR) will greatly alter littoral ecosystems, causing habitat change and loss for coastal species. Habitat loss is widely used as a measurement of the risk of extinction, but because many coastal species are migratory, the impact of habitat loss will depend not only on its extent, but also on where it occurs. Here, we develop a novel graph-theoretic approach to measure the vulnerability of a migratory network to the impact of habitat loss from SLR based on population flow through the network. We show that reductions in population flow far exceed the proportion of habitat lost for 10 long-distance migrant shorebirds using the East Asian-Australasian Flyway. We estimate that SLR will inundate 23-40% of intertidal habitat area along their migration routes, but cause a reduction in population flow of up to 72 per cent across the taxa. This magnifying effect was particularly strong for taxa whose migration routes contain bottlenecks-sites through which a large fraction of the population travels. We develop the bottleneck index, a new network metric that positively correlates with the predicted impacts of habitat loss on overall population flow. Our results indicate that migratory species are at greater risk than previously realized.

Rapid population decline in red knots: fitness consequences of decreased refuelling rates and late arrival in Delaware Bay.

Most populations of migrant shorebirds around the world are in serious decline, suggesting that vital condition-dependent rates such as fecundity and annual survival are being affected globally. A striking example is the red knot (Calidris canutus rufa) population wintering in Tierra del Fuego, which undertakes marathon 30,000 km hemispheric migrations annually. In spring, migrant birds forage voraciously on horseshoe crab eggs in Delaware Bay in the eastern USA before departing to breed in Arctic polar deserts. From 1997 to 2002 an increasing proportion of knots failed to reach threshold departure masses of 180-200 g, possibly because of later arrival in the Bay and food shortage from concurrent over-harvesting of crabs. Reduced nutrient storage, especially in late-arriving birds, possibly combined with reduced sizes of intestine and liver during refuelling, had severe fitness consequences for adult survival and recruitment of young in 2000-2002. From 1997 to 2002 known survivors in Delaware Bay were heavier at initial capture than birds never seen again, annual survival of adults decreased by 37% between May 2000 and May 2001, and the number of second-year birds in wintering flocks declined by 47%. Population size in Tierra del Fuego declined alarmingly from 51,000 to 27,000 in 2000-2002, seriously threatening the viability of this subspecies. Demographic modelling predicts imminent endangerment and an increased risk of extinction of the subspecies without urgent risk-averse management.