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.

Impact of secondary salinisation on freshwater ecosystems : effect of experimentally increased salinity on an intermittent floodplain wetland

Intermittent wetlands are particularly at risk from secondary salinisation because salts are concentrated during drawdown. We conducted a field experiment to examine the effect of adding salt at two different concentrations (to achieve nominal conductivities of 1000 μS cm–1 (low salt) and 3000 μS cm–1 (high salt)) on water quality, freshwater plants and epiphytic diatoms in an intermittent wetland during a 3.3-month drawdown. Conductivity increased to 3000 and 8500 μS cm–1 in low-salt and high-salt treatments respectively. Salt was apparently lost to the sediments, causing protons to be released from the sediments and reducing water column pH from 6.9 to 5.5 in the low-salt treatment and to 4.0 in the high-salt treatments. Forty days after adding the salt, biomass, %cover and flower production in Potamogeton cheesmanii were significantly reduced, whereas Amphibromus fluitans was not significantly affected. The salt effect on Triglochin procera was intermediate between the other two macrophytes. Significant reductions in the density, species richness and diversity of epiphytic diatoms occurred in the high-salt, but not in the low-salt, treatments. Our work shows that increases in salinity, and thus conductivity (up to 8500 μS cm–1), in low-alkalinity intermittent wetlands can change water quality, with significant adverse effects on some macrophyte and diatom communities.

Above- and below-ground vertebrate herbivory may each favour a different subordinate species in an aquatic plant community

At least two distinct trade-offs are thought to facilitate higher diversity in productive plant communities under herbivory. Higher investment in defence and enhanced colonization potential may both correlate with decreased competitive ability in plants. Herbivory may thus promote coexistence of plant species exhibiting divergent life history strategies. How different seasonally tied herbivore assemblages simultaneously affect plant community composition and diversity is, however, largely unknown. Two contrasting types of herbivory can be distinguished in the aquatic vegetation of the shallow lake Lauwersmeer. In summer, predominantly above-ground tissues are eaten, whereas in winter, waterfowl forage on below-ground plant propagules. In a 4-year exclosure study we experimentally separated above-ground herbivory by waterfowl and large fish in summer from below-ground herbivory by Bewick’s swans in winter. We measured the individual and combined effects of both herbivory periods on the composition of the three-species aquatic plant community. Herbivory effect sizes varied considerably from year to year. In 2 years herbivore exclusion in summer reinforced dominance of Potamogeton pectinatus with a concomitant decrease in Potamogeton pusillus, whereas no strong, unequivocal effect was observed in the other 2 years. Winter exclusion, on the other hand, had a negative effect on Zannichellia palustris, but the effect size differed considerably between years. We suggest that the colonization ability of Z. palustris may have enabled this species to be more abundant after reduction of P. pectinatus tuber densities by swans. Evenness decreased due to herbivore exclusion in summer. We conclude that seasonally tied above- and below-ground herbivory may each stimulate different components of a macrophyte community as they each favoured a different subordinate plant species.

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.

Swan foraging shapes spatial distribution of two submerged plants, favouring the preferred prey species

Compared to terrestrial environments, grazing intensity on belowground plant parts may be particularly strong in aquatic environments, which may have great effects on plant-community structure. We observed that the submerged macrophyte, Potamogeton pectinatus, which mainly reproduces with tubers, often grows at intermediate water depth and that P. perfoliatus, which mainly reproduces with rhizomes and turions, grows in either shallow or deep water. One mechanism behind this distributional pattern may be that swans prefer to feed on P. pectinatus tubers at intermediate water depths. We hypothesised that when swans feed on tubers in the sediment, P. perfoliatus rhizomes and turions may be damaged by the uprooting, whereas the small round tubers of P. pectinatus that escaped herbivory may be more tolerant to this bioturbation. In spring 2000, we transplanted P. perfoliatus rhizomes into a P. pectinatus stand and followed growth in plots protected and unprotected, respectively, from bird foraging. Although swan foraging reduced tuber biomass in unprotected plots, leading to lower P. pectinatus density in spring 2001, this species grew well both in protected and unprotected plots later that summer. In contrast, swan grazing had a dramatic negative effect on P. perfoliatus that persisted throughout the summer of 2001, with close to no plants in the unprotected plots and high densities in the protected plots. Our results demonstrate that herbivorous waterbirds may play a crucial role in the distribution and prevalence of specific plant species. Furthermore, since their grazing benefitted their preferred food source, the interaction between swans and P. pectinatus may be classified as ecologically mutualistic.

The role of herbivorous water birds in aquatic systems through interactions with aquatic macrophytes, with special reference to the Bewick’s Swan – Fennel Pondweed system

The role of aquatic macrophytes in stimulating biodiversity and maintaining clear waters is currently undisputed. The management of (eutrophic) shallow waters is therefore often directed at (re-)establishing macrophyte domination. In contrast, the role of water birds has long been considered of minor importance for the functioning of fresh water ecosystems. Indeed, in terms of biomass and production, water birds constitute only a minor part of these systems. However, water birds may graze heavily on water plants under certain circumstances, and the question arises whether herbivorous water birds have an important indirect effect on shallow fresh water systems. Mainly illustrated with the interaction between Bewick’s Swans and Fennel Pondweed, we present data on the role that water plants may play in the life of water birds and how water birds may impact water plants’ fitness in terms of survival, production, dispersal and competitive ability. It appears that water plants may be crucial for water birds during periods of high-energy requirements, such as migration. Despite the plants’ costs associated with water bird grazing, the interaction between water birds and water plants varies in nature from an apparent predator–prey relationship to a mutually beneficial interaction depending on the context and the perspective. For the case of the Bewick’s Swan–Fennel Pondweed interaction, regular bird grazing is sustainable and may actually favour the plant’s dispersal. Thus, Bewick’s Swans themselves may in fact play a crucial role in establishing and maintaining the Fennel Pondweed rich staging sites between the swans’ wintering and breeding grounds, which are vital for the swans’ successful migration.

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.

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.

The effect of herbivores on genotypic diversity in a clonal aquatic plant

In clonal plants, vegetative parts may outcompete seeds in the absence of disturbance, limiting the build-up of genotypic diversity through repeated seedling recruitment (RSR). Herbivory may provide disturbance and trigger establishment of strong colonizers (seeds) at the expense of strong competitors (clonal propagules). In the clonal aquatic fennel pondweed Potamogeton pectinatus, two distinct herbivore guilds may modify the dynamics of propagation. In winter, Bewick's swans may deplete patches of tubers, promoting seedling establishment in spring. In summer, seed consumption by waterfowl can reduce the density of viable seeds but grazing may also reduce tuber production and hence facilitate seedling establishment. This study is among the first to experimentally test herbivore impact on plant genotypic diversity. We assess the separate and combined effects of both herbivore guilds on genotypic diversity and structure of fennel pondweed beds. Using microsatellites, we genotyped P. pectinatus from an exclosure experiment and assessed the contribution of herbivory, dispersal and sexual reproduction to the population genetic structure. Despite the predominance of clonal propagation in P. pectinatus, we found considerable genotypic diversity. Within the experimental blocks, kinship among genets decreased with geographic distance, clearly identifying a role for RSR in the maintenance of genotypic diversity within the fennel pondweed beds. However, over a period of five years, none of the herbivory treatments affected genotypic diversity. Hence, sexual reproduction on a local scale is important in this putatively clonal plant and possibly sufficient to ensure a relatively high genotypic diversity even in the absence of herbivores. Although we cannot preclude a role of herbivory in shaping genotypic diversity of a clonal plant, after five years of exclusion of the two investigated herbivore guilds no measurable effect on genotypic diversity was detected. © 2014 The Authors.

Long-distance endozoochorous dispersal of submerged macrophyte seeds by migratory waterbirds in northern Europe - a critical review of possibilities and limitations

We review whether migratory Anatidae, i.e., swans, geese and ducks, could be acting as vectors for dispersal of Zostera, Ruppia and Potamogeton propagules by endozoochory (carrying seeds in their guts). We list six prerequisites that must all be fulfilled, if successful dispersal should occur. Several Anatidae species feed on these macrophytes, and undertake rapid long-distance movements, making dispersal possible. We identify four problems, which in combination leads us to conclude that long-distance dispersal events are likely to be rare. (i) Most long-distance movements are out of phase with the reproductive efforts of the plants, and if birds arrive at sites when plants still bear seeds, they are likely to depart well after seed stocks have been depleted. (ii) Seed transport by birds will usually be uni-directional, from north to south on autumn migrations. (iii) Most of the gut contents of migratory birds are likely to have been discarded within 300 km of departure. (iv) In many cases, birds will arrive in habitats seriously different from those they departed, i.e., any seeds carried along will have low chances of surviving in their new site. We suggest that northbound dispersal by endozoochory can only occur during spring if waterbirds feed on seeds that have not been depleted and remained frozen down or buried in sediments, or during moult- or post-moult migrations. Moult migration takes place in summer in phase with the reproductive efforts of the plants. Also epizoochorous dispersal (external attachment) is subject to restrictions i, ii and iv.

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.

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.