Relationship between wintering site and survival in a migratory waterbird using different migration routes.

When wintering at different sites, individuals from the same breeding population can experience different conditions, with costs and benefits that may have implications throughout their lifetime. Using a dataset from a longitudinal study on Eurasian Spoonbills from southern France, we explored whether survival rate varied among individuals using different wintering sites. In the last 13 years, more than 3000 spoonbills have been ringed as chicks in Camargue. These birds winter in five main regions that vary in both migratory flyway (East Atlantic vs. Central European) and migration distance (long-distance vs. short-distance vs. resident). We applied Cormack-Jolly-Seber models and found evidence for apparent survival to correlate with migration distance, but not with flyway. During the interval between the first winter sighting and the next breeding period, long-distance migrants had the lowest survival, independently of the flyway taken. Additionally, as they age, spoonbills seem to better cope with migratory challenges and wintering conditions as no differences in apparent survival among wintering strategies were detected during subsequent years. As dispersal to other breeding colonies was rarely observed, the lower apparent survival during this period is likely to be partly driven by lower true survival. This supports the potential role of crossing of natural barriers and degradation of wintering sites in causing higher mortality rates as recorded for a variety of long-distance migrants. Our work confirms variation in demographic parameters across winter distribution ranges and reinforces the importance of longitudinal studies to better understand the complex demographics of migratory species.

Low fitness at low latitudes: Wintering in the tropics increases migratory delays and mortality rates in an Arctic breeding shorebird.

Evolutionary theories of seasonal migration generally assume that the costs of longer migrations are balanced by benefits at the non-breeding destinations. We tested, and rejected, the null hypothesis of equal survival and timing of spring migration for High Arctic breeding sanderling Calidris alba using six and eight winter destinations between 55°N and 25°S, respectively. Annual apparent survival was considerably lower for adult birds wintering in tropical West Africa (Mauritania: 0.74 and Ghana: 0.75) than in three European sites (0.84, 0.84 and 0.87) and in subtropical Namibia (0.85). Moreover, compared with adults, second calendar-year sanderlings in the tropics, but not in Europe, often refrained from migrating north during the first possible breeding season. During northward migration, tropical-wintering sanderlings occurred at their final staging site in Iceland 5-15 days later than birds wintering further north or south. Namibia-wintering sanderlings tracked with solar geolocators only staged in West Africa during southward migration. The low annual survival, the later age of first northward migration and the later passage through Iceland during northward migration of tropical-wintering sanderlings, in addition to the skipping of this area during northward but not southward migration by Namibia-wintering sanderlings, all suggest they face issues during the late non-breeding season in West Africa. Migrating sanderlings defy long distances but may end up in winter areas with poor fitness prospects. We suggest that ecological conditions in tropical West Africa make the fuelling prior to northward departure problematic.

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.

Unexpected dietary preferences of Eurasian Spoonbills in the Dutch Wadden Sea: spoonbills mainly feed on small fish not shrimp.

After an historical absence, over the last decades Eurasian Spoonbills Platalea leucorodia leucorodia have returned to breed on the barrier islands of the Wadden Sea. The area offers an abundance of predator-free nesting habitat, low degrees of disturbance, and an extensive intertidal feeding area with increasing stocks of brown shrimp Crangon crangon, the assumed main prey of P. leucorodia leucorodia. Nevertheless, newly established and expanding colonies of spoonbills have surprisingly quickly reached plateau levels. Here we tested the often stated assertion that spoonbills mainly rely on brown shrimp as food, by quantifying the diet of chicks on the basis of regurgitates and by analysis of blood isotopes using stable isotope Bayesian mixing models. Both methods showed that, rather than brown shrimp being the staple food of spoonbill chicks, small flatfish (especially plaice Pleuronectes platessa) and gobies (Pomatoschistus spp.) were their main prey. Unlike shrimp, small flatfish have been reported to be rather scarce in the Wadden Sea in recent years, which may explain the rapid saturation of colony size due to food-related density-dependent recruitment declines of growing colonies. By way of their diet and colony growth characteristics, spoonbills may thus indicate the availability of small fish in the Wadden Sea. We predict that the recovery to former densities of young flatfish and other juvenile/small fish in the Wadden Sea will be tracked by changing diets (more fish) and an increase in the size of Eurasian Spoonbill colonies across the Wadden Sea.

An age-dependent fitness cost of migration? Old trans-Saharan migrating spoonbills breed later than those staying in Europe, and late breeders have lower recruitment.

Migration is a widespread phenomenon in the animal kingdom. On the basis of the considerable variation that exists between and within species, and even within populations, we may be able to infer the (age- and sex-specific) ecological trade-offs and constraints moulding migration systems from assessments of fitness associated with migration and wintering in different areas. During three consecutive breeding seasons, we compared the reproductive performance (timing of breeding, breeding success, chick body condition and post-fledging survival) of Eurasian spoonbills Platalea leucorodia that breed at a single breeding site in The Netherlands, but migrate different distances (c. 4,500 vs. 2,000 km, either or not crossing the Sahara) to and from wintering areas in southern Europe and West Africa. Using mark-recapture analysis, we further investigated whether survival until adulthood (recruitment probability) of chicks hatched between 2006 and 2010 was related to their hatch date and body condition. Long-distance migrants bred later, particularly the males, and raised chicks of poorer body condition than short-distance migrants. Hatch dates strongly advanced with increasing age in short-distance migrants, but hardly advanced in long-distance migrants, causing the difference in timing of breeding between long- and short-distance migrants to be more pronounced among older birds. Breeding success and chick body condition decreased over the season, and chicks that fledged late in the season or in poor condition were less likely to survive until adulthood. As a result, long-distance migrants-particularly the males and older birds-likely recruit fewer offspring into the breeding population than short-distance migrants. This inference is important for predicting the population-level consequences of changes in winter habitat suitability throughout the wintering range. Assuming that the long-distance migrants-being the birds that occupy the traditional wintering areas-are not the poorer quality birds, and that the observed age-dependent patterns in timing of breeding are driven by within-individual effects and not by selective disappearance, our results suggest that the strategy of long-distance migration, involving the crossing of the Sahara to winter in West Africa, incurred a cost by reducing reproductive output, albeit a cost paid only later in life.

Body shrinkage due to Arctic warming reduces red knot fitness in tropical wintering range.

Reductions in body size are increasingly being identified as a response to climate warming. Here we present evidence for a case of such body shrinkage, potentially due to malnutrition in early life. We show that an avian long-distance migrant (red knot, Calidris canutus canutus), which is experiencing globally unrivaled warming rates at its high-Arctic breeding grounds, produces smaller offspring with shorter bills during summers with early snowmelt. This has consequences half a world away at their tropical wintering grounds, where shorter-billed individuals have reduced survival rates. This is associated with these molluscivores eating fewer deeply buried bivalve prey and more shallowly buried seagrass rhizomes. We suggest that seasonal migrants can experience reduced fitness at one end of their range as a result of a changing climate at the other end.

The cost of migration: spoonbills suffer higher mortality during trans-Saharan spring migrations only.

Explanations for the wide variety of seasonal migration patterns of animals all carry the assumption that migration is costly and that this cost increases with migration distance. Although in some studies, the relationships between migration distance and breeding success or annual survival are established, none has investigated whether mortality during the actual migration increases with migration distance. Here, we compared seasonal survival between Eurasian spoonbills (Platalea leucorodia leucorodia) that breed in The Netherlands and migrate different distances (ca 1000, 2000 and 4500 km) to winter in France, Iberia and Mauritania, respectively. On the basis of resightings of individually marked birds throughout the year between 2005 and 2012, we show that summer, autumn and winter survival were very high and independent of migration distance, whereas mortality during spring migration was much higher (18%) for the birds that wintered in Mauritania, compared with those flying only as far as France (5%) or Iberia (6%). As such, this study is the first to show empirical evidence for increased mortality during some long migrations, likely driven by the presence of a physical barrier (the Sahara desert) in combination with suboptimal fuelling and unfavourable weather conditions en route.

Seasonal variation in density dependence in age-specific survival of a long-distance migrant.

Density dependence in vital rates is key to population regulation. Rather than being constant, the strength of density dependence may vary throughout the year, but empirical evidence is limited. Based on 22 years of data of color-banded birds from a recovering population of Eurasian Spoonbills Platalea leucorodia leucorodia, we show, for the first time, seasonal variation in density dependence in survival of a long-distance migrating bird. Combining resightings and dead recoveries at breeding, stopover, and nonbreeding areas enabled us to (1) separate true survival from permanent emigration from the breeding area, and (2) estimate survival in three seasons: summer, early winter (including autumn migration), and late winter (including spring migration). Accompanying the rapid population growth, juvenile annual survival initially increased, manifested in early winter, but thereafter, at high population sizes, it strongly decreased through a combination of decreasing survival in all seasons. Annual survival of subadult (second- and third-year) and adult birds decreased more gradually with increasing population size, with density dependence occurring in early winter for subadults and late winter for adults. Thus, the shape and strength of density dependence in survival varied with age and season. Understanding the seasonal timing of density dependence, especially with reference to underlying mechanisms, is important for the design of effective conservation strategies.

Toxin constraint explains diet choice, survival and population dynamics in a molluscivore shorebird.

Recent insights suggest that predators should include (mildly) toxic prey when non-toxic food is scarce. However, the assumption that toxic prey is energetically as profitable as non-toxic prey misses the possibility that non-toxic prey have other ways to avoid being eaten, such as the formation of an indigestible armature. In that case, predators face a trade-off between avoiding toxins and minimizing indigestible ballast intake. Here, we report on the trophic interactions between a shorebird (red knot, Calidris canutus canutus) and its two main bivalve prey, one being mildly toxic but easily digestible, and the other being non-toxic but harder to digest. A novel toxin-based optimal diet model is developed and tested against an existing one that ignores toxin constraints on the basis of data on prey abundance, diet choice, local survival and numbers of red knots at Banc d'Arguin (Mauritania) over 8 years. Observed diet and annual survival rates closely fit the predictions of the toxin-based model, with survival and population size being highest in years when the non-toxic prey is abundant. In the 6 of 8 years when the non-toxic prey is not abundant enough to satisfy the energy requirements, red knots must rely on the toxic alternative.

Migration tendency delays distributional response to differential survival prospects along a flyway.

When populations grow or decline, habitat selection may change due to local density-dependent processes, such as site dependence and interference. In seasonally migrating animals, nonbreeding distributions may be determined through these mechanisms of density dependence, which we examine here at a hemispheric scale for a long-distance migrating bird. Using summer and winter resightings of 2,095 Eurasian spoonbills Platalea leucorodia leucorodia that were ringed in the Netherlands during 16 years of fast population growth, we show that neither site dependence nor interference fully explains their patterns of survival and winter distribution. Within their three main wintering areas, annual survival decreased with an increase in population size. While survival was consistently higher in the two European wintering areas (France, Iberia), most spoonbills migrated onward to winter in west Africa. The number of birds wintering in Europe increased, but not enough to maximize annual survival. We conclude that a constraint of tradition (their "migration tendency") inhibits birds from changing their migratory habits. We pose that this phenomenon may similarly constrain other migratory populations from rapidly responding to large-scale climate- and/or human-driven habitat changes at their wintering grounds.