Longer guts and higher food quality increase energy intake in migratory swans

1.  Within the broad field of optimal foraging, it is increasingly acknowledged that animals often face digestive constraints rather than constraints on rates of food collection. This therefore calls for a formalization of how animals could optimize food absorption rates.

2.  Here we generate predictions from a simple graphical optimal digestion model for foragers that aim to maximize their (true) metabolizable food intake over total time (i.e. including nonforaging bouts) under a digestive constraint.

3.  The model predicts that such foragers should maintain a constant food retention time, even if gut length or food quality changes. For phenotypically flexible foragers, which are able to change the size of their digestive machinery, this means that an increase in gut length should go hand in hand with an increase in gross intake rate. It also means that better quality food should be digested more efficiently.

4.  These latter two predictions are tested in a large avian long-distance migrant, the Bewick's swan (Cygnus columbianus bewickii), feeding on grasslands in its Dutch wintering quarters.

5.  Throughout winter, free-ranging Bewick's swans, growing a longer gut and experiencing improved food quality, increased their gross intake rate (i.e. bite rate) and showed a higher digestive efficiency. These responses were in accordance with the model and suggest maintenance of a constant food retention time.

6.  These changes doubled the birds’ absorption rate. Had only food quality changed (and not gut length), then absorption rate would have increased by only 67%; absorption rate would have increased by only 17% had only gut length changed (and not food quality).

7.  The prediction that gross intake rate should go up with gut length parallels the mechanism included in some proximate models of foraging that feeding motivation scales inversely to gut fullness. We plea for a tighter integration between ultimate and proximate foraging models.

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 Bewick's 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.

Time and energy constraints in demanding phases of the annual cycle : an example of time limitation in refuelling migratory swans

The daily metabolizable energy intake of an animal is potentially limited by either the available feeding time or by its capacity to process energy. Animals are generally considered not to be time-limited but rather to be energy-processing-limited. This is concluded from the common observation that an animal's feeding time per day increases with a decrease in food density. We argue that such changes in feeding time are in theory also expected when no constraints are operating. Thus, a study of the constraints on energy intakes of free-living animals should be performed during demanding phases of the year. As an example, we collected data on time and energy budgets of Bewick's swan (Cygnus columbianus bewickii) refuelling during migration on fennel pondweed (Potamogeton pectinatus) tubers in two years differing two-fold in tuber biomass density. As predicted by time limitation, the feeding time (defined as the time with the head submerged) did not change in response to a change in food biomass density, both within and between years (averaging 12.2 h d⁻¹). Contrary to energy-processing limitation, and again in line with time limitation, the daily metabolizable energy intake varied, being greater in the year with high than in the year with low food densities. We conclude that more studies are needed of animals operating under demanding conditions before it can be assessed whether free-living animals are generally energy-processing- or time-limited.

A puzzling migratory detour : are fueling conditions in Alaska driving the movement of juvenile sharp-tailed sandpipers?

Making a detour can be advantageous to a migrating bird if fuel-deposition rates at stopover sites along the detour are considerably higher than at stopover sites along a more direct route. One example of an extensive migratory detour is that of the Sharp-tailed Sandpiper (Calidris acuminata), of which large numbers of juveniles are found during fall migration in western Alaska. These birds take a detour of 1500-3400 km from the most direct route between their natal range in northeastern Siberia and nonbreeding areas in Australia. We studied the autumnal fueling rates and fuel loads of 357 Sharp-tailed Sandpipers captured in western Alaska. In early September the birds increased in mass at a rate of only 0.5% of lean body mass day^-1. Later in September, the rate of mass increase was about 6% of lean body mass day^-1, among the highest values found among similar-sized shorebirds around the world. Some individuals more than doubled their body mass because of fuel deposition, allowing nonstop flight of between 7100 and 9800 km, presumably including a trans-oceanic flight to the southern hemisphere. Our observations indicated that predator attacks were rare in our study area, adding another potential benefit of the detour. We conclude that the most likely reason for the Alaskan detour is that it allows juvenile Sharp-tailed Sandpipers to put on large fuel stores at exceptionally high rates.

Host behaviour and physiology underpin individual variation in avian influenza virus infection in migratory Bewick's swans

Individual variation in infection modulates both the dynamics of pathogens and their impact on host populations. It is therefore crucial to identify differential patterns of infection and understand the mechanisms responsible. Yet our understanding of infection heterogeneity in wildlife is limited, even for important zoonotic host-pathogen systems, owing to the intractability of host status prior to infection. Using novel applications of stable isotope ecology and eco-immunology, we distinguish antecedent behavioural and physiological traits associated with avian influenza virus (AIV) infection in free-living Bewick's swans (Cygnus columbianus bewickii). Swans infected with AIV exhibited higher serum δ13C (-25.3 ± 0.4) than their non-infected counterparts (-26.3±0.2). Thus, individuals preferentially foraging in aquatic rather than terrestrial habitats experienced a higher risk of infection, suggesting that the abiotic requirements of AIV give rise to heterogeneity in pathogen exposure. Juveniles were more likely to be infected (30.8% compared with 11.3% for adults), shed approximately 15-fold higher quantity of virus and exhibited a lower specific immune response than adults. Together, these results demonstrate the potential for heterogeneity in infection to have a profound influence on the dynamics of pathogens, with concomitant impacts on host habitat selection and fitness.

Comparing the seasonal survival of resident and migratory oystercatchers : carry-over effects of habitat quality and weather conditions

Events happening in one season can affect life-history traits at (the) subsequent season(s) by carry-over effects. Wintering conditions are known to affect breeding success, but few studies have investigated carry-over effects on survival. The Eurasian oystercatcher Haematopus ostralegus is a coastal wader with sedentary populations at temperate sites and migratory populations in northern breeding grounds of Europe. We pooled continental European ringing-recovery datasets from 1975 to 2000 to estimate winter and summer survival rates of migrant and resident populations and to investigate long-term effects of winter habitat changes. During mild climatic periods, adults of both migratory and resident populations exhibited survival rates 2% lower in summer than in winter. Severe winters reduced survival rates (down to 25% reduction) and were often followed by a decline in survival during the following summer, via short-term carry-over effects. Habitat changes in the Dutch wintering grounds caused a reduction in food stocks, leading to reduced survival rates, particularly in young birds. Therefore, wintering habitat changes resulted in long-term (>10 years) 8.7 and 9.4% decrease in adult annual survival of migrant and resident populations respectively. Studying the impact of carry-over effects is crucial for understanding the life history of migratory birds and the development of conservation measures.

Experimental quantification of long distance dispersal potential of aquatic snails in the gut of migratory birds

Many plant seeds and invertebrates can survive passage through the digestive system of birds, which may lead to long distance dispersal (endozoochory) in case of prolonged retention by moving vectors. Endozoochorous dispersal by waterbirds has nowadays been documented for many aquatic plant seeds, algae and dormant life stages of aquatic invertebrates. Anecdotal information indicates that endozoochory is also possible for fully functional, active aquatic organisms, a phenomenon that we here address experimentally using aquatic snails. We fed four species of aquatic snails to mallards (Anas platyrhynchos), and monitored snail retrieval and survival over time. One of the snail species tested was found to survive passage through the digestive tract of mallards as fully functional adults. Hydrobia (Peringia) ulvae survived up to five hours in the digestive tract. This suggests a maximum potential transport distance of up to 300 km may be possible if these snails are taken by flying birds, although the actual dispersal distance greatly depends on additional factors such as the behavior of the vectors. We put forward that more organisms that acquired traits for survival in stochastic environments such as wetlands, but not specifically adapted for endozoochory, may be sufficiently equipped to successfully pass a bird's digestive system. This may be explained by a digestive trade-off in birds, which maximize their net energy intake rate rather than digestive efficiency, since higher efficiency comes with the cost of prolonged retention times and hence reduces food intake. The resulting lower digestive efficiency allows species like aquatic snails, and potentially other fully functional organisms without obvious dispersal adaptations, to be transported internally. Adopting this view, endozoochorous dispersal may be more common than up to now thought.

Unravelling migratory connectivity in marine turtles using multiple methods

1. Comprehensive knowledge of the fundamental spatial ecology of marine species is critical to allow the identification of key habitats and the likely sources of anthropogenic threats, thus informing effective conservation strategies. 2. Research on migratory marine vertebrates has lagged behind many similar terrestrial animal groups, but studies using electronic tagging systems and molecular techniques offer great insights. 3. Marine turtles have complex life history patterns, spanning wide spatio-temporal scales. As a result of this multidimensional complexity, and despite extensive effort, there are no populations for which a truly holistic understanding of the spatial aspects of the life history has been attained. There is a particular lack of information regarding the distribution and habitats utilized during the first few years of life. 4. We used satellite tracking technology to track individual turtles following nesting at the green turtle Chelonia mydas nesting colony at Poilão Island, Guinea Bissau; the largest breeding aggregation in the eastern Atlantic. 5. We further contextualize these data with pan-Atlantic molecular data and oceanographic current modelling to gain insights into likely dispersal patterns of hatchlings and small pelagic juveniles. 6. All adult turtles remained in the waters of West Africa, with strong connectivity demonstrated with Banc D’Arguin, Mauritania. 7. Despite shortcomings in current molecular markers, we demonstrate evidence for profound sub-structuring of marine turtle stocks across the Atlantic; with a high likelihood based on oceanographic modelling that most turtles from Guinea-Bissau are found in the eastern Atlantic. 8. Synthesis and applications. There is an increased need for a better understanding of spatial distribution of marine vertebrates demonstrating life histories with spatio-temporal complexity. We propose the synergistic use of the technologies and modelling used here as a working framework for the future rapid elucidation of the range and likely key habitats used by the different life stages from such species.

Indicators of the impact of climate change on migratory species

The Bonn Convention on the Conservation of Migratory Species of Wild Animals adopted a Resolution in 2005 recognising the impacts of climate change on migratory species. It called on Contracting Parties to undertake more research to improve our understanding of these impacts and to implement adaptation measures to reduce foreseeable adverse effects. Given the large diversity of taxa and species affected by climate change, it is impossible to monitor all species and effects thereof. However, it is likely that many of the key ecological and physical processes through which climate change may impact wildlife could be monitored using a suite of indicators, each comprising parameters of species/populations or groups of species as proxies for wider assemblages, habitats and ecosystems. Herein, we identify a suite of 17 indicators whose attributes could reveal negative impacts of climate change on the global status of migratory species: 4 for birds, 4 for marine mammals, 2 for sea turtles, 1 for fish, 3 for land mammals and 3 for bats. A few of these indicators would be relatively straightforward to develop, but most would require additional data collation, and in many cases methodological development. Choosing and developing indicators of the impacts of climate change on migratory species is a challenge, particularly with endangered species, which are subject to many other pressures. To identify and implement conservation measures for these species, indicators must account for the full ensemble of pressures, and link to a system of alerts and triggers for action.

Travelling through a warming world: climate change and migratory species

Long-distance migrations are among the wonders of the natural world, but this multi-taxon review shows that the characteristics of species that undertake such movements appear to make them particularly vulnerable to detrimental impacts of climate change. Migrants are key components of biological systems in high latitude regions, where the speed and magnitude of climate change impacts are greatest. They also rely on highly productive seasonal habitats, including wetlands and ocean upwellings that, with climate change, may become less food-rich and predictable in space and time. While migrants are adapted to adjust their behaviour with annual changes in the weather, the decoupling of climatic variables between geographically separate breeding and non-breeding grounds is beginning to result in mistimed migration. Furthermore, human land-use and activity patterns will constrain the ability of many species to modify their migratory routes and may increase the stress induced by climate change. Adapting conservation strategies for migrants in the light of climate change will require substantial shifts in site designation policies, flexibility of management strategies and the integration of forward planning for both people and wildlife. While adaptation to changes may be feasible for some terrestrial systems, wildlife in the marine ecosystem may be more dependent on the degree of climate change mitigation that is achievable.

A review of migratory behaviour of sea turtles off southeastern Africa

The survival of sea turtles is threatened by modern fishing methods, exploitation of eggs and habitat destruction. Forming keystone species in the ocean, their extinction would disrupt the marine food chain in ways as yet unknown. The Indian Ocean has many breeding areas for sea turtles, the southernmost ones being on the Maputaland coast of KwaZulu-Natal, where loggerhead and leatherback turtles nest in large numbers thanks to long-lasting protection programmes. For the leatherback this is the only known nesting site in the entire western Indian Ocean. At the end of the reproductive season, both loggerheads and leatherbacks undertake migrations towards disparate feeding areas. To contribute to their conservation, the migratory behaviour of these animals needs to be understood. Here we review 10 years studying this behaviour using transmitters that telemeter data via satellite. It emerges that these species frequent widely dispersed areas ranging from the Atlantic Ocean to the Mozambique Channel. The migratory behaviour of leatherback and loggerhead turtles is, however, very different, probably due to their differing food requirements. While loggerhead postnesting movements have a truly migratory nature, the large-scale wanderings of leatherbacks are better described as prolonged sojourns in extended feeding areas.