Jan A. van Gils

Hampered Foraging and Migratory Performance in Swans Infected with Low-Pathogenic Avian Influenza A Virus

It is increasingly acknowledged that migratory birds, notably waterfowl, play a critical role in the maintenance and spread of influenza A viruses. In order to elucidate the epidemiology of influenza A viruses in their natural hosts, a better understanding of the pathological effects in these hosts is required. Here we report on the feeding and migratory performance of wild migratory Bewicks swans (Cygnus columbianus bewickii Yarrell) naturally infected with low-pathogenic avian influenza (LPAI) A viruses of subtypes H6N2 and H6N8. Using information on geolocation data collected from Global Positioning Systems fitted to neck-collars, we show that infected swans experienced delayed migration, leaving their wintering site more than a month after uninfected animals. This was correlated with infected birds travelling shorter distances and fuelling and feeding at reduced rates. The data suggest that LPAI virus infections in wild migratory birds may have higher clinical and ecological impacts than previously recognised.

A Three-Stage Symbiosis Forms the Foundation of Seagrass Ecosystems

Ancient Associations Submarine seagrass meadows are critical to fisheries and coastline protection and provide feeding grounds for many endangered species, including dugongs and turtles, and serve as a nursery for coral reef fish. The persistence and maintenance of seagrass ecosystems have been mysterious, because accumulation of organic matter in the beds should rapidly lead to toxic sulphide levels in the sediment. Using a meta-analysis and a field study, van der Heide et al. (p. 1432) atttribute the 100-million-year success of seagrasses to a three-stage symbiosis. Seagrass beds worldwide contain high densities of small lucinid bivalves that have symbiotic sulphide-oxidizing bacteria in their gills. This association appears to relieve any sulphide stress for seagrasses, while the lucinids and their symbionts profit from the accumulation of degradable organic matter and oxygen release from seagrass roots. A marine plant, small molluscs, and their resident sulfide-oxidizing bacteria survive together. Seagrasses evolved from terrestrial plants into marine foundation species around 100 million years ago. Their ecological success, however, remains a mystery because natural organic matter accumulation within the beds should result in toxic sediment sulfide levels. Using a meta-analysis, a field study, and a laboratory experiment, we reveal how an ancient three-stage symbiosis between seagrass, lucinid bivalves, and their sulfide-oxidizing gill bacteria reduces sulfide stress for seagrasses. We found that the bivalve–sulfide-oxidizer symbiosis reduced sulfide levels and enhanced seagrass production as measured in biomass. In turn, the bivalves and their endosymbionts profit from organic matter accumulation and radial oxygen release from the seagrass roots. These findings elucidate the long-term success of seagrasses in warm waters and offer new prospects for seagrass ecosystem conservation.

Incompletely informed shorebirds that face a digestive constraint maximize net energy gain when exploiting patches

Foragers that feed on hidden prey are uncertain about the intake rate they can achieve as they enter a patch. However, foraging success can inform them, especially if they have prior knowledge about the patch quality distribution in their environment. We experimentally tested whether and how red knots (Calidris canutus) use such information and whether their patch‐leaving decisions maximized their long‐term net energy intake rate. The results suggest that the birds combined patch sample information with prior knowledge by making use of the potential value assessment rule. We reject five alternative leaving rules. The potential encounter rate that the birds choose as their critical departure threshold maximized their foraging gain ratio (a modified form of efficiency) while foraging. The high experimental intake rates were constrained by rate of digestion. Under such conditions, maximization of the foraging gain ratio during foraging maximizes net intake rate during total time (foraging time plus digestive breaks). We conclude that molluscivore red knots, in the face of a digestive constraint, are able to combine prior environmental knowledge about patch quality with patch sample information to obtain the highest possible net intake over total time.

Shellfish Dredging Pushes a Flexible Avian Top Predator out of a Marine Protected Area

There is a widespread concern about the direct and indirect effects of industrial fisheries; this concern is particularly pertinent for so-called “marine protected areas” (MPAs), which should be safeguarded by national and international law. The intertidal flats of the Dutch Wadden Sea are a State Nature Monument and are protected under the Ramsar convention and the European Unions Habitat and Birds Directives. Until 2004, the Dutch government granted permission for ~75% of the intertidal flats to be exploited by mechanical dredgers for edible cockles (Cerastoderma edule). Here we show that dredged areas belonged to the limited area of intertidal flats that were of sufficient quality for red knots (Calidris canutus islandica), a long-distance migrant molluscivore specialist, to feed. Dredging led to relatively lower settlement rates of cockles and also reduced their quality (ratio of flesh to shell). From 1998 to 2002, red knots increased gizzard mass to compensate for a gradual loss in shellfish quality, but this compensation was not sufficient and led to decreases in local survival. Therefore, the gradual destruction of the necessary intertidal resources explains both the loss of red knots from the Dutch Wadden Sea and the decline of the European wintering population. This study shows that MPAs that do not provide adequate protection from fishing may fail in their conservation objectives.

Reinterpretation of gizzard sizes of red knots world-wide emphasises overriding importance of prey quality at migratory stopover sites

The size of digestive organs can be rapidly and reversibly adjusted to ecological circumstances, but such phenotypic flexibility comes at a cost. Here, we test how the gizzard mass of a long-distance migrant, the red knot (Calidris canutus), is adjusted to (i) local climate, (ii) prey quality and (iii) migratory fuelling demands. For eight sites around the world (both wintering and stopover sites), we assembled data on gizzard masses of free-living red knots, the quality of their prey and the local climate. Using an energetic cost–benefit approach, we predicted the gizzard size required for fastest fuelling (net rate-maximization, i.e. expected during migration) and the gizzard size required to balance daily energy budgets (satisficing, expected in wintering birds) at each site. The measured gizzards matched the net rate-maximizing predictions at stopover sites and the satisficing predictions at wintering sites. To our surprise, owing to the fact that red knots selected stopover sites with prey of particularly high quality, gizzard sizes at stopovers and at wintering sites were nevertheless similar. To quantify the benefit of minimizing size changes in the gizzard, we constructed a model incorporating the size-dependent energy costs of maintaining and carrying a gizzard. The model showed that by selecting stopovers containing high-quality prey, metabolic rates are kept at a minimum, potentially reducing the spring migratory period by a full week. By inference, red knots appear to time their stopovers so that they hit local peaks in prey quality, which occur during the reproductive seasons of the intertidal benthic invertebrates.

High-tide habitat choice: insights from modelling roost selection by shorebirds around a tropical bay

High tides force shorebirds from intertidal feeding areas to sites known as roosts. We investigated the roost selection of great knots, Calidris tenuirostris, and red knots, Calidris canutus, on a tropical coastline in northwestern Australia, assessing several roost attributes and recording the frequency of use of each site through automatic radiotelemetry. To model roost choice we used two approaches: (1) conditional logistic regression models that assumed roost selection to be a trade-off based on a probabilistic assessment of several environmental characteristics; and (2) bounds-based models that assumed that birds selected the nearest roost site to their feeding grounds, provided that threshold values for certain environmental characteristics were met. Bounds-based models were more effective, and we suggest that they offer a closer approach to real roost choice mechanisms. By day, roost choice was affected by distance from the feeding area and microclimate; birds selected nearby roosts where they could stand on cool, wet substrates. Different roost selection criteria were used at night when birds chose safer, but more distant, roosts. Models that assumed that roost choice was influenced by recent experience of roost sites performed better than models that assumed constant assessment of roost quality. This effect was significant only at night, suggesting that memory was used more when information on roost quality was limited. Evidence that roost availability may influence selection of foraging areas is also presented. Our results suggest that shorebirds select roosts by using simple mechanisms, making roost choice models a potentially valuable tool in conservation planning.

Cost-benefit analysis of mollusc eating in a shorebird I: Foraging and processing costs estimated by the doubly labelled water method

SUMMARY Although the energy costs of foraging and food processing in vertebrates may be considerable, they have rarely been quantified separately. Here we present estimates for both cost factors based on a series of trials with a shorebird, the red knot Calidris canutus, fed natural and artificial prey types under naturalistic but fully controlled indoor aviary conditions. During eight 1-day trials we successfully manipulated the extent to which the five red knots were (1) actively probing and walking (i.e. foraging) and (2) actually ingesting prey (i.e. processing food) that was (3) either hard-shelled or not (i.e. crushing). Energy expenditures, estimated by the doubly labelled water (DLW) method, calibrated for use in this particular condition, varied between 1.5 and 4 W. A hierarchical analysis of variance indicated that the crushing of hard-shelled prey entailed no extra cost. We arrived at the following breakdown of cost components under the thermoneutral conditions of the experiment: a cost of active rest/maintenance of 1.665 W, an additional cost of foraging of 0.602 W and an additional digestive processing cost of 1.082 W. These cost levels are all well within the range of expectation and are consistent with the results of a separate outdoor aviary experiment in which the thermostatic costs needed separate estimation. On the basis of the cost and performance functions of gizzards of different mass, it was shown that under the conditions of this experiment the red knots expended the bare minimum for a balanced budget, maintaining the smallest possible gizzard. Under field conditions a larger gizzard would be required.

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

Consequences conferred at a distance Migratory animals have adapted to life in multiple, sometimes very different environments. Thus, they may show particularly complex responses as climates rapidly change. Van Gils et al. show that body size in red knot birds has been decreasing as their Arctic breeding ground warms (see the Perspective by Wikelski and Tertitski). However, the real toll of this change appears not in the rapidly changing northern part of their range but in the apparently more stable tropical wintering range. The resulting smaller, short-billed birds have difficulty reaching their major food source, deeply buried mollusks, which decreases the survival of birds born during particularly warm years. Science, this issue p. 819; see also p. 775 A warming Arctic decreases the fitness of migratory red knots in their distant 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.

Reversed optimality and predictive ecology: burrowing depth forecasts population change in a bivalve.

Optimality reasoning from behavioural ecology can be used as a tool to infer how animals perceive their environment. Using optimality principles in a ‘reversed manner’ may enable ecologists to predict changes in population size before such changes actually happen. Here we show that a behavioural anti-predation trait (burrowing depth) of the marine bivalve Macoma balthica can be used as an indicator of the change in population size over the year to come. The per capita population growth rate between years t and t+1 correlated strongly with the proportion of individuals living in the dangerous top 4 cm layer of the sediment in year t: the more individuals in the top layer, the steeper the population decline. This is consistent with the prediction based on optimal foraging theory that animals with poor prospects should accept greater risks of predation. This study is among the first to document fitness forecasting in animals.

Scaling up ideals to freedom : Are densities of Red Knots across western Europe consistent with ideal free distribution?

Local studies have shown that the distribution of red knots Calidris canutus across intertidal mudflats is consistent with the predictions of an ideal distribution, but not a free distribution. Here, we scale up the study of feeding distributions to their entire wintering area in western Europe. Densities of red knots were compared among seven wintering sites in The Netherlands, UK and France, where the available mollusc food stocks were also measured and from where diets were known. We tested between three different distribution models that respectively assumed (i) a uniform distribution of red knots over all areas, (ii) a uniform distribution across all suitable habitat (based on threshold densities of harvestable mollusc prey), and (iii) an ideal and free distribution (IFD) across all suitable habitats. Red knots were not homogeneously distributed across the different European wintering areas, also not when considering suitable habitats only. Their distribution was best explained by the IFD model, suggesting that the birds are exposed to interference and have good knowledge about their resource landscape at the spatial scale of NW Europe, and that the costs of movement between estuaries, at least when averaged over a whole winter, are negligible.