The exception to the rule : Retreating ice front makes Bewick's swans Cygnus columbianus bewickii migrate slower in spring than in autumn

In the vast majority of migratory bird species studied so far, spring migration has been found to proceed faster than autumn migration. In spring, selection pressures for rapid migration are purportedly higher, and migratory conditions such as food supply, daylength, and/or wind support may be better than in autumn. In swans, however, spring migration appears to be slower than autumn migration. Based on a comparison of tundra swan Cygnus columbianus tracking data with long-term temperature data from wheather stations, it has previously been suggested that this was due to a capital breeding strategy (gathering resources for breeding during spring migration) and/or to ice cover constraining spring but not autumn migration. Here we directly test the hypothesis that Bewick's swans Cygnus columbianus bewickii follow the ice front in spring, but not in autumn, by comparing three years of GPS tracking data from individual swans with concurrent ice cover data at five important migratory stop-over sites. In general, ice constrained the swans in the middle part of spring migration, but not in the first (no ice cover was present in the first part) nor in the last part. In autumn, the swans migrated far ahead of ice formation, possibly in order to prevent being trapped by an early onset of winter. We conclude that spring migration in swans is slower than autumn migration because spring migration speed is constrained by ice cover. This restriction to spring migration speed may be more common in northerly migrating birds that rely on freshwater resources. © 2013 The Authors.

Skipping swans: fuelling rates and wind conditions determine differential use of migratory stopover sites of Bewick's Swans Cygnus bewickii

Some migratory birds refuel at stopover sites that they by-pass on the return trip. In theory, this skipping behaviour is only expected in time-selected migrants when the overflown site is of a lower quality than the departure site. We provide empirical evidence that quality differences in stopover sites are the cause for skipping in Bewick's Swans Cygnus bewickii tracked by satellite telemetry. Two and five complete tracks were recorded in spring and autunm, respectively, showing that the White Sea was visited for c. 2 weeks in spring, but by-passed (or visited for a few days at the most) in autumn. Skipping of the White Sea in autumn was predicted by a dynamic programming model which was based on calculated gain rates during stopover in the Pechora Delta and the White Sea. This prediction was not sensitive to plausible variations in gain rates. Relative to the Pechora Delta the White Sea is a poor site because a large tidal amplitude precludes foraging on the beds of the submerged macrophyte Fennel Pondweed Potamogeton pectinatus during high tide. The dynamic programming model predicted a fast autunm migration. However, the phenology of autunm arrival dates of Bewick's Swans on the wintering grounds revealed that only in three out of ten years a significant number of birds was able to reach the wintering grounds without refuelling. In the other years, unfavourable wind conditions along the Russian/Baltic part of the route prevented such non-stop migration.

Insights from the eco-physiological book of records : Bewick's swans outperform the canonical intake-maximizing vertebrate

During periods of high energy demand an animal may be constrained by a physiological maximum to its energy intake rate. Predictions by allometric equations describing this maximum for endotherms were significantly surpassed during a few recent laboratory experiments on birds and mammals, being given access to food 24 h day^-1. How relevant this is in the field remains to be assessed. We predicted that Bewick’s swans Cygnus columbianus bewickii might surpass this maximum during stopover on their migration. We determined intake rate by measuring initial and final biomass density, and dividing the biomass difference by the feeding time required to reach this difference. This feeding time was given by the functional response. After conversion to daily energy intake rates, these exceeded the previously assumed maximum on two of the three stopover sites studied. The exception was a stopover site where daily foraging time was limited by the tidal cycle. Our study confirms that intake rates may exceed the formerly generally supposed maximum under natural conditions when foraging is possible day and night.

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.

Compensatory growth in an aquatic plant mediates exploitative competition between seasonally tied herbivores

The degree to which vertebrate herbivores exploitatively compete for the same food plant may depend on the level of compensatory plant growth. Such compensation is higher when there is reduced density-dependent competition in plants after herbivore damage. Whether there is relief from competition may largely be determined by the life-history stage of plants under herbivory. Such stage-specific compensation may apply to seasonal herbivory on the clonal aquatic plant sago pondweed (Potamogeton pectinatus L.). It winters in sediments of shallow lakes as tubers that are foraged upon by Bewick's Swans (Cygnus columbianus bewickii Yarrell), whereas aboveground biomass in summer is mostly consumed by ducks, coots, and Mute Swans. Here, tuber predation may be compensated due to diminished negative density dependence in the next growth season. However, we expected lower compensation to summer herbivory by waterfowl and fish as density of aboveground biomass in summer is closely related to photosynthetic carbon fixation. In a factorial exclosure study we simultaneously investigated (1) the effect of summer herbivory on aboveground biomass and autumn tuber biomass and (2) the effect of tuber predation in autumn on aboveground biomass and tuber biomass a year later. Summer herbivory strongly influenced belowground tuber biomass in autumn, limiting food availability to Bewick's Swans. In contrast, tuber predation in autumn by Bewick's Swans had a limited and variable effect on P. pectinatus biomass in the following growth season. Whereas relief from negative density dependence largely eliminates effects of belowground herbivory by swans, aboveground herbivory in summer limits both above- and belowground plant biomass. Hence, there was an asymmetry in exploitative competition, with herbivores in summer reducing food availability for belowground herbivores in autumn, but not the other way around.

Burial depth distribution of fennel pondweed tubers (Potamogeton pectinatus) in relation to foraging by Bewick's swans

Deep burial in the sediment of tubers of fennel pondweed (Potamogeton pectinatus) has been explained in terms of avoidance by escape against consumption by Bewick's swans (Cygnus columbianus bewickii) in autumn. We therefore expected changes in foraging pressure to ultimately result in a change in the tuber distribution across sediment depth. A trade-off underlies this idea: deep tubers are less accessible to swans but must be larger to meet the higher energy demands of sprouting in spring. To test this prediction, we compared tuber burial depth over a gradient of foraging pressure both across space and across time. Tuber samples were obtained after aboveground plant senescence but before arrival of Bewick's swans. First, we compared the current tuber bank depth profile in a shallow lake with high foraging pressure, the Lauwersmeer, with that in two wetlands with moderate and low foraging pressure. Second, we compared the current tuber burial in the Lauwersmeer with that in the early 1980s when exploitation by swans had just started there. In accordance with our hypothesis, we found significantly deeper burial of tubers under high consumption risk compared to low consumption risk, both when comparing sites and comparing time periods. Since tubers in effect only survive to the next spring, the observed differences in burial depth among sites and over time cannot be a direct result of tuber losses due to consumption by swans. Rather, these observations suggest adaptive responses in tuber burial related to foraging pressure from Bewick's swans in the recent past. We thus propose that fennel pondweed exhibits flexible avoidance by escape, of a kind rarely described for plants, where both phenotypic plasticity and genotype sorting may contribute to the observed differences in tuber burial.

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.

Animal–plant–microbe interactions : direct and indirect effects of swan foraging behaviour modulate methane cycling in temperate shallow wetlands

Wetlands are among the most important ecosystems on Earth both in terms of productivity and biodiversity, but also as a source of the greenhouse gas CH₄. Microbial processes catalyzing nutrient recycling and CH₄ production are controlled by sediment physico-chemistry, which is in turn affected by plant activity and the foraging behaviour of herbivores. We performed field and laboratory experiments to evaluate the direct effect of herbivores on soil microbial activity and their indirect effects as the consequence of reduced macrophyte density, using migratory Bewick’s swans (Cygnus columbianus bewickii Yarrell) feeding on fennel pondweed (Potamogeton pectinatus L.) tubers as a model system. A controlled foraging experiment using field enclosures indicated that swan bioturbation decreases CH₄ production, through a decrease in the activity of methanogenic Archaea and an increased rate of CH₄ oxidation in the bioturbated sediment. We also found a positive correlation between tuber density (a surrogate of plant density during the previous growth season) and CH₄ production activity. A laboratory experiment showed that sediment sterilization enhances pondweed growth, probably due to elimination of the negative effects of microbial activity on plant growth. In summary, the bioturbation caused by swan grazing modulates CH₄ cycling by means of both direct and indirect (i.e. plant-mediated) effects with potential consequences for CH₄ emission from wetland systems.

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.

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.

Aquatic plant shows flexible avoidance by escape from tuber predation by swans

Deeper burial of bulbs and tubers has been suggested as an escape against below-ground herbivory by vertebrates, but experimental evidence is lacking. As deep propagule burial can incur high costs of emergence after dormancy, burial depth may represent a trade-off between sprouting survival and herbivore avoidance. We tested whether burial depth of subterraneous tubers is a flexible trait in fennel pondweed (Potamogeton pectinatus), facing tuber predation by Bewick's swans (Cygnus columbianus bewickii) in shallow lakes in winter. In a four-year experiment involving eight exclosures, winter herbivory by swans and all vertebrate summer herbivory were excluded in a full-factorial design; we hence controlled for aboveground vertebrate herbivory in summer, possibly influencing tuber depth. Tuber depth was measured each September before swan arrival and each March before tuber sprouting. In accordance with our hypothesis, tuber depth in September decreased after excluding Bewick's swans in comparison to control plots. The summer exclosure showed an increase in tuber biomass and the number of shallow tubers, but not a significant effect on the mean burial depth of tuber mass. Our results suggest that a clonal plant like P. pectinatus can tune the tuber burial depth to predation pressure, either by phenotypic plasticity or genotype sorting, hence exhibiting flexible avoidance by escape. We suggest that a flexible propagule burial depth can be an effective herbivore avoidance strategy, which might be more widespread among tuber forming plant species than previously thought.

Habitat use throughout migration : linking individual consistency, prior breeding success and future breeding potential

1. Habitat use can influence individual performance in a wide range of animals, either immediately or through carry-over effects in subsequent seasons. Given that many animal species also show consistent individual differences in reproductive success, it seems plausible that individuals may have consistent patterns of habitat use representing individual specializations, with concomitant fitness consequences.

2. Stable-carbon isotope ratios from a range of tissues were used to discern individual consistency in habitat use along a terrestrial–aquatic gradient in a long-distance migrant, the Bewick’s swan (Cygnus columbianus bewickii). These individual specialisations represented <15% of the isotopic breadth of the population for the majority of individuals and were seen to persist throughout autumn migration and overwintering until aquatic habitats were no longer available.

3. Individual foraging specialisations were then used to demonstrate two consecutive carry-over effects associated with macroscale habitat segregation: consequences of breeding season processes for autumn habitat use; and consequences of autumn habitat use for future reproductive success. Adults that were successful breeders in the year of capture used terrestrial habitats significantly more than adults that were not successful, revealing a substantial cost of reproduction and extended parental care. Use of aquatic habitats during autumn was, however, associated with increased body condition prior to spring migration; and increased subsequent breeding success in adults that had been unsuccessful the year before. Yet adults that were successful breeders in the year of capture remained the most likely to be successful the following year, despite their use of terrestrial habitats.

4. Our results uniquely demonstrate not only individual foraging specializations throughout the migration period, but also that processes during breeding and autumn migration, mediated by individual consistency, may play a fundamental role in the population dynamics of long-distance migrants. These findings, therefore, highlight the importance of long-term consistency to our understanding of habitat function, interindividual differences in fitness, population dynamics and the evolution of migratory strategies.

Migrating swans profit from favourable changes in wind conditions at low altitude

Because energy reserves limit flight range, wind assistance may be of crucial importance for migratory birds. We tracked eight Bewick's swans Cygnus columbianus bewickii, using 95-g satellite transmitters with altimeters and activity sensors, during their spring migration from Denmark to northern Russia in 1996. During the 82 occasions where a swan's location was recorded in flight, average flight altitude was 165 m a.s.1. with a maximum of 759 m a.s.1., despite winds often being more favourable at higher altitudes. We also counted Bewick's swans departing from the Gulf of Finland and subsequently passing an observatory in the next major stop-over area 800 km further north in the White Sea, northern Russia, during the springs of 1994, 1995 and 1996. A comparison of these counts with wind data provided evidence for Bewick's swans using favourable changes in wind conditions to embark on migration. Changes in the numbers of birds arriving in the White Sea correlated best with favourable changes in winds in the Gulf of Finland 1 day earlier. Again, migratory volume showed a correlation with winds at low altitudes only, despite wind conditions for the swans being more favourable at high altitudes. We conclude that the relatively large Bewick's swan tends to gear its migration to wind conditions at low altitude only. We argue that Bewick's swans do not climb to high altitudes because of mechanical and physiological limitations with respect to the generation of power for flight and to avoid rapid dehydration.

Spatial variation in tuber depletion by swans explained by differences in net intake rates

We tested whether the spatial variation in resource depletion by Tundra Swans (Cygnus columbianus) foraging on belowground tubers of sago pondweed (Potamogeton pectinatus) was caused by differences in net energy intake rates. The variation in giving-up densities within the confines of one lake was nearly eightfold, the giving-up density being positively related to water depth and, to a lesser extent, the silt content of the sediment. The swans' preference (measured as cumulative foraging pressure) was negatively related to these variables. We adjusted a model developed for diving birds to predict changes in the time allocation of foraging swans with changes in power requirements and harvest rate. First, we compared the behavior of free-living swans foraging in shallow and deep water, where they feed by head-dipping and up-ending, respectively. Up-ending swans had 1.3-2.1 times longer feeding times than head-dipping swans. This was contrary to our expectation, since the model predicted a decrease in feeding time with an increase in feeding power. However, up-ending swans also had 1.9 times longer trampling times than headdipping swans. The model predicted a strong positive correlation between trampling time and feeding time, and the longer trampling times may thus have masked any effect of an increase in feeding power. Heart rate measurements showed that trampling was the most energetically costly part of foraging. However, because the feeding time and trampling time changed concurrently, the rate of energy expenditure was only slightly higher in deep water (1.03-1.06 times). This is a conservative estimate since it does not take into account that the feeding costs of up-ending are possibly higher than that of head-dipping. Second, we compared captive swans foraging on sandy and clayey sediments. We found that the harvest rate on clayey sediment was only 0.6 times that on sandy sediment and that the power requirements for foraging were 1.2-1.4 times greater. Our results are in qualitative agreement with the hypothesis that the large spatial variation in giving-up densities was caused by differences in net rates of energy intake. This potentially has important implications for the prey dynamics, because plant regrowth has been shown to be related to the same habitat factors (water depth and sediment type).

Habitat switching by Bewick's swans: Maximization of average long-term energy gain?

1. In a system where depletion drives a habitat shift, the hypothesis was tested that animals switch habitat as soon as the average daily net energy intake (or gain) drops below that attainable in the alternative habitat.

2. The study was performed in the Lauwersmeer area. Upon arrival during the autumn migration, Bewick's swans first feed on below-ground tubers of fennel pondweed on the lake, but subsequently switched to feeding on harvest remains in sugar beet fields.

3. The daily energy intake was estimated by multiplying the average time spent foraging per day with the instantaneous energy intake rate while foraging. In the case of pondweed feeding, the latter was estimated from the functional response and the depletion of tuber biomass. In the case of beet feeding, it was estimated from dropping production rate. Gross energy intake was converted to metabolizable energy intake using the assimilation as determined in digestion trials. The daily energy expenditure was estimated by the time-energy budget method. Energetic costs were determined using heart rate.

4. The daily gain of pondweed feeding at the median date of the habitat switch (i.e. when 50% of the swans had switched) was compared with that of beet feeding. The daily gain of beet feeding was calculated for two strategies depending on the night activity on the lake: additional pondweed feeding (mixed feeding) or sleeping (pure beet feeding).

5. The majority of the swans switched when the daily gain they could achieve by staying on the pondweed bed fell just below the average daily gain of pure beet feeders. However, mixed feeders would attain an average daily gain considerably above that of pondweed feeders. A sensitivity analysis showed that this result was robust.

6. We therefore reject the hypothesis that the habitat switch by swans can be explained by simple long-term energy rate maximization. State-dependency, predation risk, and protein requirements are put forward as explanations for the delay in habitat switch.