Site fidelity of migratory shorebirds facing habitat deterioration: insights from satellite tracking and mark-resighting.

BACKGROUND: Site fidelity, the tendency to return to a previously visited site, is commonly observed in migratory birds. This behaviour would be advantageous if birds returning to the same site, benefit from their previous knowledge about local resources. However, when habitat quality declines at a site over time, birds with lower site fidelity might benefit from a tendency to move to sites with better habitats. As a first step towards understanding the influence of site fidelity on how animals cope with habitat deterioration, here we describe site fidelity variation in two species of sympatric migratory shorebirds (Bar-tailed Godwits Limosa lapponica and Great Knots Calidris tenuirostris). Both species are being impacted by the rapid loss and deterioration of intertidal habitats in the Yellow Sea where they fuel up during their annual long-distance migrations. METHODS: Using satellite tracking and mark-resighting data, we measured site fidelity in the non-breeding (austral summer) and migration periods, during which both species live and co-occur in Northwest Australia and the Yellow Sea, respectively. RESULTS: Site fidelity was generally high in both species, with the majority of individuals using only one site during the non-breeding season and revisiting the same sites during migration. Nevertheless, Great Knots did exhibit lower site fidelity than Bar-tailed Godwits in both Northwest Australia and the Yellow Sea across data types. CONCLUSIONS: Great Knots encountered substantial habitat deterioration just before and during our study period but show the same rate of decline in population size and individual survival as the less habitat-impacted Bar-tailed Godwits. This suggests that the lower site fidelity of Great Knots might have helped them to cope with the habitat changes. Future studies on movement patterns and their consequences under different environmental conditions by individuals with different degrees of site fidelity could help broaden our understanding of how species might react to, and recover from, local habitat deterioration.

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.

Thermal adaptation best explains Bergmann's and Allen's Rules across ecologically diverse shorebirds.

Bergmann's and Allen's rules state that endotherms should be larger and have shorter appendages in cooler climates. However, the drivers of these rules are not clear. Both rules could be explained by adaptation for improved thermoregulation, including plastic responses to temperature in early life. Non-thermal explanations are also plausible as climate impacts other factors that influence size and shape, including starvation risk, predation risk, and foraging ecology. We assess the potential drivers of Bergmann's and Allen's rules in 30 shorebird species using extensive field data (>200,000 observations). We show birds in hot, tropical northern Australia have longer bills and smaller bodies than conspecifics in temperate, southern Australia, conforming with both ecogeographical rules. This pattern is consistent across ecologically diverse species, including migratory birds that spend early life in the Arctic. Our findings best support the hypothesis that thermoregulatory adaptation to warm climates drives latitudinal patterns in shorebird size and shape.

Unravelling the processes between phenotypic plasticity and population dynamics in migratory birds.

Populations can rapidly respond to environmental change via adaptive phenotypic plasticity, which can also modify interactions between individuals and their environment, affecting population dynamics. Bird migration is a highly plastic resource-tracking tactic in seasonal environments. However, the link between the population dynamics of migratory birds and migration tactic plasticity is not well-understood. The quality of staging habitats affects individuals' migration timing and energy budgets in the course of migration and can consequently affect individuals' breeding and overwintering performance, and impact population dynamics. Given staging habitats being lost in many parts of the world, our goal is to investigate responses of individual migration tactics and population dynamics in the face of loss of staging habitat and to identify the key processes connecting them. We started by constructing and analysing a general full-annual-cycle individual-based model with a stylized migratory population to generate hypotheses on how changes in the size of staging habitat might drive changes in individual stopover duration and population dynamics. Next, through the interrogation of survey data, we tested these hypotheses by analysing population trends and stopover duration of migratory waterbirds experiencing the loss of staging habitat. Our modelling exercise led to us posing the following hypotheses: the loss of staging habitat generates plasticity in migration tactics, with individuals remaining on the staging habitat for longer to obtain food due to a reduction in per capita food availability. The subsequent increasing population density on the staging habitat has knock-on effects on population dynamics in the breeding and overwintering stage. Our empirical results were consistent with the modelling predictions. Our results demonstrate how environmental change that impacts one energetically costly life-history stage in migratory birds can have population dynamic impacts across the entire annual cycle via phenotypic plasticity.

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.

Draft Genome Sequences of Four Citrobacter Isolates Recovered from Wild Australian Shorebirds.

Citrobacter is a ubiquitous bacterial genus whose members inhabit a variety of niches. Some species are clinically important for both antimicrobial resistance (AMR) carriage and as the cause of nosocomial infections. Surveillance of Citrobacter species in the environment can provide indicators of the spread of AMR genes outside clinical spaces. In this study, we present draft genome sequences of four Citrobacter isolates obtained from three species of wild Australian shorebirds.

Accounting for heterogeneity when estimating stopover duration, timing and population size of red knots along the Luannan Coast of Bohai Bay, China.

To successfully perform their long-distance migrations, migratory birds require sites along their migratory routes to rest and refuel. Monitoring the use of so-called stopover and staging sites provides insights into (a) the timing of migration and (b) the importance of a site for migratory bird populations. A recently developed Bayesian superpopulation model that integrates mark-recapture data and ring density data enabled the estimation of stopover timing, duration, and population size. Yet, this model did not account for heterogeneity in encounter (p) and staying (ϕ) probabilities.Here we extended the integrated superpopulation model by implementing finite mixtures to account for heterogeneity in p and ϕ. We used simulations and real data (from 2009-2016) on red knots Calidris canutus, mostly of the subspecies piersmai, staging in Bohai Bay, China, during spring migration to (a) show the importance of accounting for heterogeneity in encounter and staying probabilities to get unbiased estimates of stopover timing, duration, and numbers of migratory birds at staging sites and (b) get accurate stopover parameter estimates for a migratory bird species at a key staging site that is threatened by habitat destruction.Our simulations confirmed that heterogeneity in p affected stopover parameter estimates more than heterogeneity in ϕ, especially when most birds had low p. Bias was particularly severe when most birds had both low ϕ and p. Bias was largest for population size, intermediate for stopover duration and negligible for stopover timing.A total of 50,000-100,000 red knots were estimated to annually stop for 5-9 days in Bohai Bay between 10 and 30 May. This shows the key importance of this staging site for this declining species. There were no clear changes in stopover parameters over time, although stopover population size was substantially lower in 2016 than in preceding years.Our study shows the importance of accounting for heterogeneity in both encounter and staying probabilities for accurately estimating stopover duration and population size and provides an appropriate modeling framework.

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.