Anne Dekinga

Empirical evidence for differential organ reductions during trans–oceanic bird flight

Since the early 1960s it has been held that migrating birds deposit and use only fat as fuel during migratory flight, with the non–fat portion of the body remaining homeostatic. Recent evidence from field studies has shown large changes in organ sizes in fuelling birds, and theory on fuel use suggests protein may be a necessary fuel during flight. However, an absence of information on the body condition of migrants before and after a long flight has hampered understanding of the dynamics of organs during sustained flight. We studied body condition in a medium–sized shorebird, the great knot (Calidris tenuirostris), before and after a flight of 5400 km from Australia to China during northward migration. Not only did these birds show the expected large reduction in fat content after migration, there was also a decrease in lean tissue mass, with significant decreases in seven organs. The reduction in functional components is reflected in a lowering of the basal metabolic rate by 46%. Recent flight models have tried to separate the ‘flexible’ part of the body from the constant portion. Our results suggest that apart from brains and lungs no organs are homeostatic during long–distance flight. Such organ reductions may be a crucial adaptation for long–distance flight in birds.

Interactions between stomach structure and diet choice in shorebirds

Captive Red Knots (Calidris canutus) fed soft food pellets developed atrophied stomachs, and were reluctant to eat their usual hard-shelled mollusc prey. An interspecific comparison among shorebirds showed that wild Red Knots and other intact-mollusc-eating species have gizzards with relatively great mass but very small proventriculi. Within six different shorebird species, the heavier individuals usually had the heavier stomachs as well, but in Red Knots and Bar-tailed Godwits (Limosa lapponica) we identified heavy premigrant individuals with reduced stomach masses, suggesting a reallocation of protein reserves before long-distance flights. In both species reduced stomach mass was associated with a relatively soft diet. We were unable to show that during adjustment of stomachs to hard-shelled prey, such prey are broken down to smaller fragments. We attribute this to the counteractive influence of the pylorus during adjustment. We summarize the suggested stomach/diet interactions as a network of causal relationships and feedback loops involving the type of diet and gizzard mass. We identify two basic modifiers of gizzard mass: one working via endurance training and disuse atrophy; and another involving endocrine and/or neural mechanisms. It is likely that, in the course of their annual cycle, shorebirds are prevented from achieving maximal digestive performance owing to seasonal changes in feeding habitats and diet enforced by their long-distance migrations.

Scale and intensity of intertidal habitat use by knots Calidris canutus in the Western Wadden Sea in relation to food, friends and foes

Abstract In August–October 1988–1992 we studied the distribution and abundance of knots Calidris canutus around Griend in the western Wadden Sea, and the extent to which these can be explained by benthic prey availability and presence of avian predators. Numbers in the nonbreeding season showed monthly averages of 10 000 to 25 000 birds. Over 100 000 knots were recorded on three occassions. Knots feed in large flocks, individual birds usually experiencing 4 000 to 15 000 flock-mates. The Siberian-breeding/west-African wintering canutus subspecies passed through in late July and early August. Otherwise the Greenlandic/Canadian breeding islandica subspecies was present. Over the period 1964–1992 there were no clear trends in the number of knots, but canutus -knots were particularly abundant in July–August 1991, whereas in 1992 both subspecies were absent. Macoma balthica was the preferred prey of both subspecies. Hydrobia ulvae, Mytilus edulis and Cerastoderma edule were eaten when Macoma was absent close to the surface of the sediment. As Macoma buried deeper from July onwards, canutus faced better average feeding conditions than islandica later in the year. The spatial distributon of knots feeding on the intertidal flats around Griend was best explained by the harvestable biomass of the prevalent prey species in a particular year and season, i.e. Macoma (main prey when their harvestable biomass densities were greater than ca 0.8 g AFDM per m 2 ) and Cerastoderma , and by the avoidance of situations where they run the risk of attack by bird-eating birds. Flocks of knots covered most of the intertidal flats in the Western Dutch Wadden Sea in a couple of tidal cycles. This is about 800 km 2 , much larger than the equivalent area used by knots on their wintering grounds in Mauritania (10–15 km 2 ), a difference that is correlated with prey spectrum, prey availability and predictability.

Acclimation to different thermal conditions in a northerly wintering shorebird is driven by body mass-related changes in organ size

SUMMARY Seasonal acclimatization and experimental acclimation to cold in birds typically results from increased shivering endurance and elevated thermogenic capacity leading to improved resistance to cold. A wide array of physiological adjustments, ranging from biochemical transformations to organ mass variations, are involved in this process. Several studies have shown that improved cold endurance is accompanied by increases in summit metabolic rate (Msum), a measure of maximal heat production and an indicator of the level of sustainable thermogenic capacity. However, improved endurance to cold can also be achieved without significant changes in Msum. The same is true for basal metabolic rate (BMR), which is known to increase in association with cold acclimatization or acclimation in some species but not in others. We investigated cold acclimation in a migrant shorebird known for extreme physiological flexibility, the red knot (Calidris canutus, the northerly wintering subspecies islandica). We measured BMR and Msum over two months in birds caught in the wild and transferred to experimentally controlled conditions representative of aspects of their seasonal thermal environment (two groups at constant 25°C, one group at constant 4°C and two groups experiencing variable outdoor temperatures). Birds maintained in both cold and variable ambient temperatures showed a 14-15% higher body mass, 33-45% higher food intake, and 26% and 13% elevations in BMR and Msum, respectively, compared with birds kept at thermoneutrality. These results, together with data on alimentary tract size and pectoral muscle thickness measured by ultrasonography, suggest that red knots acclimate to cold primarily through modulation of (lean) body mass components. Heavier individuals have larger muscles, which allow higher maximal heat production and better thermal compensation. Cold acclimation effects on BMR are most probably due to changes in the size of visceral organs, although not the alimentary tract in this specific case. The liver, known for its thermogenic capacity, is a probable candidate. Overall, our results indicate that relatively small changes in body mass and muscle size allow enough reserve capacity in terms of heat production to cope with typical wintering ambient temperature variations as measured on the red knots wintering grounds.

Reconstructing diet composition on the basis of faeces in a mollusc-eating wader, the Knot Calidris canutus

Methods are described to assess the molluscan diet of Knots feeding on intertidal flats in western Europe from their faecal output. The size distributions of two common bivalve prey, Macoma balthica and Cerastoderma edule, can be estimated from the heights of shell hinges retrieved from droppings. The average ingested size of the tiny mudsnail Hydrobia ulvae can be reconstructed from partially broken shells. Diet composition in terms of biomass can be estimated by a two-step procedure. First, the diet composition in terms of ash or shell mass is estimated on the basis of the sieved mass of droppings. The application of the site-, season- and size-specific ratios of biomass/shell mass or biomass/ash mass then provides a breakdown of diet with respect to biomass. An exploratory field study in the Wadden Sea showed that measurable fragments in (rarely encountered) regurgitates overestimate prey size. According to the faecal analysis, there was a seasonal change in diet from bivalves to mudsnails with the app...

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.

Mass mortality of common eiders (Somateria mollissima) in the Dutch Wadden Sea, winter 1999/2000: starvation in a commercially exploited wetland of international importance

Mass mortality of common eiders (Somateria mollissima) was observed in winter 1999/2000 in the Dutch Wadden Sea. Approximately 21,000 common eiders died. Dissected birds were severely emaciated and 94% were infected with the acanthocephalan parasite Profilicollis botulus. Green shore crabs (Carcinus maenas), intermediate hosts of the parasite, were slightly more ‘available’ than in other years, but parasite infections in the eiders were close to normal. Few eiders were oiled (5%), there were no toxicological, bacteriological, or virological explanations for the observed mortality. In the Wadden Sea, a wetland of international importance, mussel (Mytilus edulis) cultures occur in sublittoral areas, while mechanical cockle (Cerastoderma edule) fisheries are licensed annually after evaluation of available resources. The wintering eiders in 1999/2000 required c. 3.1 million kg ash-free dry mass, while information on mussel and cockle stocks (irrespective of accessibility and profitability) suggested a resource 4.7� the requirement of common eiders only. Food shortage is suggested to have caused the observed mortality, involving both principal (mussels and cockles) and secondary (Spisula) prey. Winter census reports showed shifts in wintering distribution of common eiders in the 1990s, indicating the utilisation of Spisula in the North Sea in poor food years in the Wadden Sea. Following particularly intense fisheries in summer 1999, attempts to feed on Spisula in winter 1999/2000 failed. It is hypothesised that overfishing of mussels and cockles in the Wadden Sea in the early 1990s resulted in structurally reduced food resources, contractions of the foraging area of common eiders, and increased use of secondary prey in the North Sea. # 2002 Elsevier Science Ltd. All rights reserved.

Is Long‐Distance Bird Flight Equivalent to a High‐Energy Fast? Body Composition Changes in Freely Migrating and Captive Fasting Great Knots

We studied changes in body composition in great knots, Calidris tenuirostris, before and after a migratory flight of 5,400 km from northwest Australia to eastern China. We also took premigratory birds into captivity and fasted them down to their equivalent arrival mass after migration to compare organ changes and nutrient use in a low‐energy‐turnover fast with a high‐energy‐turnover fast (migratory flight). Migrated birds were as economical as any fasting animal measured yet at conserving protein: their estimated relative protein contribution (RPC) to the energy used was 4.0%. Fasted birds had an estimated RPC of 6.8% and, consequently, a much lower lean mass and higher fat content for an equivalent body mass than migrated birds. Lean tissue was catabolized from most organs in both groups, except the brain. Furthermore, a principal components biplot showed that individuals were grouped primarily on the basis of overall organ fat or lean tissue content rather than by the size of specific organs. This indicates that organ changes during migratory flight are similar to those of a low‐energy fast, although the length of the fast in this study probably accentuated organ reductions in some functional groups. Whether the metabolic characteristics of a flying migratory fast follow the three‐phase model described in many inactive fasting animals is unclear. We have some evidence for skeletal fat being catabolized without phase 3 of a fast having been reached.

Estimating organ size in small migrating shorebirds with ultrasonography : An intercalibration exercise

Organs, even of fully grown adult birds, mammals, and reptiles, may show substantial size changes in relation to specific performances. These changes are difficult to study, because measurements usually can only be obtained following the death of the animal. We explored the use of ultrasonographic imaging, a relatively simple noninvasive technique, to measure size of pectoral muscles and stomach in two small shorebird species (red knots Calidris canutus and golden plovers Pluvialis apricaria). Accuracy of ultrasound measurements in estimating organ mass in red knots was reasonably high. Depending on the equipment used, the error of individual measurements was 20%–25% for the pectoral muscles and 26%–44% for the stomach. In plovers the technique was less accurate, probably because of the low variability of the organs involved. Ultrasound scanning is particularly suited to measure rapidly changing organ sizes over short time intervals. We demonstrate this with an example in which changes in individuals in size of pectoral muscle and stomach were monitored in captive red knots following a change in diet. Ultrasound measures will enable studies on the links between body composition and future behavior and physiology.

Dredging for edible cockles (Cerastoderma edule) on intertidal flats : short-term consequences of fisher patch-choice decisions for target and non-target benthic fauna

Intertidal flats in the Dutch Wadden Sea are protected by national and international treaties. Still, mechanical dredging for edible cockles Cerastoderma edule was allowed in 74% of 1200 km(2) of interticlal flats. Cumulatively, between 1992 and 2001, 19% of the intertidal area was affected by mechanical cockle-dredging at least once. On the basis of a grid of 2650 stations sampled annually, we evaluate the extent to which cockle-dredging from 1998 to 2003 was selective with respect to non-target macrozoobenthic intertidal fauna. In all 4 years that comparisons could be made, to-be-dredged areas contained greater diversity of macrobenthic animals than areas that remained undredged. Targeted cockles were 2.5 times more abundant in areas that were to be dredged shortly, but other species also occurred in higher densities in these areas. Small amphipods and some bivalves occurred less in to-be-dredged areas than elsewhere. In terms of short-term responses to dredging, four non-target species showed a significant decrease in abundance 1 year after dredging. Only Tellina tenuis showed an increase a year after dredging.