Liesbeth Bakker

Land-water transition areas play an important role in the functioning of both aquatic and terrestrial ecosystems. Enhancing habitat complexity and heterogeneity by restoring or adding land–water transition areas to degraded aquatic ecosystems can be effective management to stimulate productivity by lower trophic levels – and hence increase food availability for biota of conservation interest, including fish and birds. Here, we studied whether hydrological connectivity can be used as an environmental indicator (connected or disconnected) for the development trajectories of newly constructed land–water transition areas in shallow lakes. We capitalized on a large-scale restoration project called “Marker Wadden”, which created new land–water transition areas with and without hydrological connectivity in a degraded shallow lake in the Netherlands (Lake Markermeer). We compared how the new areas with and without hydrological connectivity developed with respect to abiotic parameters and biomasses of benthic, pelagic, and emergent macroinvertebrates. In sites disconnected from the open water, water depths became significantly lower than in hydrologically connected sites during summer, likely due to evaporation. In these shallower waters, daytime temperatures and organic matter content of the sediment were higher, while dissolved oxygen concentrations remained sufficient. Therefore, biomasses of benthic macroinvertebrates and emergent insects became higher in the disconnected sites. These lower trophic levels could provide higher food availability for benthivorous and insectivorous birds, while remaining inaccessible to fish. This puts forward that hydrological connectivity (connected or disconnected) can be used as an environmental indicator for aquatic food web development trajectories, and that it regulates relative food availability for fish and birds. Restoring land–water transition areas without hydrological connectivity provides higher biomasses of lower trophic levels, which are only accessible to birds. Restoring areas with hydrological connectivity results in relatively lower biomasses of invertebrates, but these provide food to birds feeding on invertebrates, and fish and fish-eating birds. Creating areas including both types of land–water transition zones, connected and disconnected to open water can benefit fish and birds of both feeding guilds.

Aim: There is increasing interest in open-ended restoration with the focus on restoring natural processes rather than static compositional goals. Here, we investigated vegetation dynamics in response to three decades of trophic rewilding with large herbivores in a recent anthropogenic, fertile 55-km² landscape on reclaimed marine sediments. This site provides important insights into plant community assembly in rewilded, young ecosystems. Location: Oostvaardersplassen, the Netherlands. Methods: Using field surveys and vegetation data spanning two decades, we investigate vegetation dynamics of the mesic grasslands in Oostvaardersplassen, a pioneer trophic rewilding site in the Netherlands. To identify the effects of grazing and other ecological processes, we include comparisons to an adjacent ungrazed control site and to the dark diversity, that is, missing species expected to be present given the environment and geography. Results: The impact of large herbivores has led to a more open and homogenous vegetation with higher plant species richness in the mesic grasslands of Oostvaardersplassen compared to the ungrazed control. Compared to species in the dark diversity, the species present are more common in the region, more stress-tolerant, and less competitive, in line with joint effects of grazing and immigrational lag. Conclusions: The changes in vegetation composition and structure show that rewilding with large herbivores promotes the prevalence of stress-tolerant and low-statured plant species, which are in decline in the broader landscape while reducing the dominance of otherwise widespread, competition-adapted species. The absence of numerous rare species suggests that dispersal limitation poses an important constraint for the diversity build-up in anthropogenically isolated natural areas, necessitating active species introductions to mitigate this issue in the short to medium term.

Human-induced nutrient eutrophication is a major threat to grassland biodiversity, because it promotes the dominance of fast-growing plants. Negative impacts of fertilization on plant biodiversity may be offset by grazing by large vertebrate herbivores. However, whether grazers also mitigate impacts of nutrient addition on insects is less well understood. We use a field experiment to test how plant communities and abundances of pollinators and grasshoppers respond to nutrient addition and grazing by different assemblages of large herbivores, i.e. access by all herbivores (including cattle and horses), access by wild herbivores only (wild boar and deer), no access by large herbivores. Plant biomass increased, plant diversity decreased and community composition shifted towards lower forb cover in response to fertilization, but only in the absence of all herbivores. Flower visitation by Hymenoptera (bees and wasps), i.e. the most abundant pollinator group, was reduced by nutrient addition only in the absence of all herbivores and was positively related to flowering plant richness. In contrast, flower visitation by Diptera (e.g. hoverflies) was enhanced by fertilization, but not affected by grazing. Orthoptera (grasshopper) abundance was reduced by grazing and enhanced by nutrient addition, with positive impacts of fertilization tending to be stronger in plots with only wild or no herbivores. The abundance of grasshoppers was positively related to grass biomass. We conclude that vertebrate herbivores can offset impacts of fertilization on both plant and insect communities, making grazing by large mammals an essential tool to protect insects, particularly pollinators. Most responses to nutrient addition were only apparent in plots without any large herbivores, suggesting that wild herbivores alone could already mitigate nutrient impacts. We also show that insects with contrasting feeding guilds may be favoured by fertilized, ungrazed conditions. Therefore, creating a mosaic of patches grazed at different intensities will enhance overall insect biodiversity.

Land-water transition areas play a significant role in the functioning of aquatic ecosystems. However, anthropogenic pressures are posing severe threats on land-water transition areas, which leads to degradation of the ecological integrity of many lakes worldwide. Enhancing habitat complexity and heterogeneity by restoring land-water transition areas in lake systems is deemed a suitable method to restore lakes bottom-up by stimulating lower trophic levels. Stimulating productivity of lower trophic levels (phytoplankton, zooplankton) generates important food sources for declining higher trophic levels (fish, birds). Here, we study ecosystem restoration project Marker Wadden in Lake Markermeer, The Netherlands. This project involved the construction of a 700-ha archipelago of five islands in a degrading shallow lake, aiming to create additional sheltered land-water transition areas to stimulate food web development from its base by improving phytoplankton quantity and quality. We found that phytoplankton quantity (chlorophyll-a concentration) and quality (inversed carbon:nutrient ratio) in the shallow waters inside the Marker Wadden archipelago were significantly improved, likely due to higher nutrient availabilities, while light availability remained sufficient, compared to the surrounding lake. Higher phytoplankton quantity and quality was positively correlated with zooplankton biomass, which was higher inside the archipelago than in the surrounding lake due to improved trophic transfer efficiency between phytoplankton and zooplankton. We conclude that creating new land-water transition areas can be used to increase light and nutrient availabilities and thereby enhancing primary productivity, which in turn can stimulate higher trophic levels in degrading aquatic ecosystems.

The success of invasive macrophytes can depend on local nutrient availability and consumer pressure, which may interact. We therefore experimentally investigated the interacting effects of nutrient (nitrogen and phosphorus) addition, the exclusion of large herbivorous fishes and mimicked grazing on the expansion rates of the invasive seagrass Halophila stipulacea. The experiments were established on Bonaire and Aruba, two islands in the southern Caribbean, which differ in fish community structure. We observed that multiple Caribbean fish species feed on H. stipulacea. At both study sites, nutrient enrichment decreased invasive leaf carbon:nitrogen ratios. However only on Bonaire, where herbivore fish abundance was 7 times higher and diversity was 4.5 times higher, did nutrient enrichment result in a significant reduction of H. stipulacea expansion into native Thalassia testudinum meadows. This effect was likely due to increased herbivory on nutrient enriched seagrass leaves, as we found that excluding large herbivorous fish (e.g. parrotfish) doubled invasive expansion rates in bare patches on Bonaire. On Aruba, H. stipulacea expansion rates were higher overall, which coincided with lower abundances and diversity of native fishes, and were limited by mimicked fish grazing. We suggest that top-down control by the native fish community may counteract eutrophication effects by increased grazing pressure on nutrient-rich invasive seagrass leaves. We conclude that diverse and abundant herbivore communities likely play an important role in limiting invasion success and their conservation and restoration may serve as a tool to slow down seagrass invasions.

Ecological models predict that the effects of mammalian herbivore exclusion on plant diversity depend on resource availability and plant exposure to ungulate grazing over evolutionary time. Using an experiment replicated in 57 grasslands on six continents, with contrasting evolutionary history of grazing, we tested how resources (mean annual precipitation and soil nutrients) determine herbivore exclusion effects on plant diversity, richness and evenness. Here we show that at sites with a long history of ungulate grazing, herbivore exclusion reduced plant diversity by reducing both richness and evenness and the responses of richness and diversity to herbivore exclusion decreased with mean annual precipitation. At sites with a short history of grazing, the effects of herbivore exclusion were not related to precipitation but differed for native and exotic plant richness. Thus, plant species’ evolutionary history of grazing continues to shape the response of the world’s grasslands to changing mammalian herbivory.

Wind-induced turbulence can strongly impact ecological processes in shallow lake ecosystems. The creation of shelter against wind can be expected to affect both primary producers and herbivores in aquatic food webs. Shelter may benefit particular primary producers more than others by changing relative resource availabilities for different primary producers. Herbivore community compositions may be affected either directly or indirectly as a consequence of changes in their food quantity and quality that, in turn, may affect the transfer efficiency between primary producers and herbivores. A reduction in trophic transfer efficiency resulting from wind-induced turbulence potentially can lead to declines of higher trophic levels, but is generally understudied. Here, we focus on the impact of wind on aquatic primary producers and trophic transfer efficiency. We hypothesised that reducing wind-induced turbulence will stimulate higher trophic production in shallow lakes. However, the multitude of impacts of wind-induced turbulence on aquatic food webs make it challenging to predict the direction of change when creating sheltered conditions. We tested our hypothesis in the shallow waters of a newly constructed archipelago named Marker Wadden in lake Markermeer in the Netherlands. Lake Markermeer has experienced declining numbers of birds and fish. These declines have been related to wind-induced sediment resuspension that potentially limits primary production and trophic transfer efficiency. Marker Wadden is a large-scale restoration project that aims to add sheltered and heterogeneous habitat to the otherwise mostly homogeneous lake, thus targeting the potential problems associated with wind-induced turbulence. We executed a 2-month manipulative field mesocosm experiment in the shallow waters of Marker Wadden to study the effect of reduced wind-induced turbulence (i.e., shelter) on aquatic food webs. Specifically, we studied the effects on primary producers, trophic transfer efficiency between phytoplankton and zooplankton (using zooplankton biomass divided by phytoplankton Chl a as a proxy), and benthic fauna. The experiment consisted of three treatments: no shelter, shelter without macrophytes and shelter with submerged macrophytes (Myriophyllum spicatum) present at the start of the experiment. Our results clearly showed that under unsheltered conditions phytoplankton was the dominant primary producer, whereas in sheltered conditions submerged macrophytes became dominant. Interestingly, submerged macrophytes appeared rapidly in the sheltered treatment where first no macrophytes were visibly present; hence, at the end of the experiment, there was little difference among the sheltered treatments with and without initial presence of submerged macrophytes. Despite that phytoplankton concentrations were 23-fold higher under the unsheltered conditions, this did not result in higher zooplankton biomass. This can be explained by a five-fold greater trophic transfer efficiency between phytoplankton and zooplankton under the sheltered conditions. Furthermore, under the sheltered conditions the Gastropoda density reached 746 individuals m⁻², whereas no Gastropoda were found under the no shelter treatment. These findings indicate that for shallow lakes that are negatively affected by wind-induced turbulence, measures aimed at ameliorating this stressor can be effective in facilitating submerged macrophyte recovery, increasing Gastropoda densities and restoring trophic transfer efficiency between phytoplankton and zooplankton. Ultimately, this may support higher trophic levels such as fish and water birds by increasing their food availability in shallow lake ecosystems.

Construction of artificial wave shelters is a promising measure to stimulate submerged vegetation in large wind exposed lakes. Here we tested whether the construction of shelter results in the colonization of submerged vegetation and whether grazing by waterbirds hampers vegetation development under those sheltered conditions. We studied the effect of breakwaters that were constructed between 1992 and 1996 in the large (695 km²), wind exposed and turbid Lake Markermeer, The Netherlands. We used monitoring data to evaluate the development of submerged vegetation and its relation with the abundance of herbivorous birds and conducted a field grazer exclosure experiment to determine the effect of grazers on the newly established vegetation. We found that in the sheltered area, a dense charophyte dominated vegetation developed over 16 years, while submerged vegetation remained very sparse outside the breakwaters. The area also attracted many herbivorous birds, especially molting Mute swans during summer. After the breakwaters had been completed, 10 years passed before the development of the charophyte vegetation started. This delay was probably not caused by bird grazing, but more likely due to unfavorable light conditions in the first decade. The exclosure experiment confirmed that while grazing reduced macrophyte biomass by 50% and plant height by 45%, it did not affect vegetation cover, which remained high (90–95%) throughout summer. The water depth in most of the study area exceeded the depth range at which Mute swans prefer to forage and this probably prevented overgrazing. We conclude that building artificial wave shelters is an effective measure to stimulate submerged vegetation in large wind exposed lakes.

Understanding how megaherbivores incorporate habitat features into their foraging behavior is key toward understanding how herbivores shape the surrounding landscape. While the role of habitat structure has been studied within the context of predator–prey dynamics and grazing behavior in terrestrial systems, there is a limited understanding of how structure influences megaherbivore grazing in marine ecosystems. To investigate the response of megaherbivores (green turtles) to habitat features, we experimentally introduced structure at two spatial scales in a shallow seagrass meadow in The Bahamas. Turtle density increased 50-fold (to 311 turtles ha⁻¹) in response to the structures, and turtles were mainly grazing and resting (low vigilance behavior). This resulted in a grazing patch exceeding the size of the experimental setup (242 m²), with reduced seagrass shoot density and aboveground biomass. After structure removal, turtle density decreased and vigilance increased (more browsing and shorter surfacing times), while seagrass within the patch partly recovered. Even at a small scale (9 m²), artificial structures altered turtle grazing behavior, resulting in grazing patches in 60% of the plots. Our results demonstrate that marine megaherbivores select habitat features as foraging sites, likely to be a predator refuge, resulting in heterogeneity in seagrass bed structure at the landscape scale.

Wetlands provide vital services on which human societies depend. As they have been rapidly degrading due to anthropogenic impacts worldwide, wetland restoration is increasingly applied. When a return to the original state of a wetland is constrained, forward-looking restoration can provide a new way to enhance an ecosystem's ecological integrity. However, the direction in which new ecosystems will develop is strongly coupled to the initial environmental conditions and may benefit from active decisions on (future) management. To improve the natural values of a degrading freshwater lake in the Netherlands, a forward-looking restoration project was initiated in lake Markermeer in 2016, involving the construction of a 700-ha archipelago called the “Marker Wadden”. This archipelago should provide new habitat to higher trophic levels in the lake's food web through the development of currently missing Common reed (Phragmites australis) dominated marshlands with gradual land-water transitions. However, the restoration project faces strong grazing pressure by Greylag geese (Anser anser) that possibly inhibit reed establishment. Here, we aimed to unravel the effect of herbivory by Greylag geese (using exclosures) and the introduction of reed rhizomes on early vegetation development and carbon dynamics on the bare soils of this new ecosystem in a manipulative field experiment. Our results showed that excluding herbivores strongly increased reed-vegetation cover, density and maximum height, but only when reed rhizomes were actively introduced. Spontaneous vegetation development on bare soils was limited, and colonization by Broadleaf cattail (Typha latifolia) dominated over reed. Net ecosystem exchange of carbon and ecosystem respiration were strongly linked to vegetation development, with highest methane emissions in the most densely vegetated plots. We conclude that the establishment of reed marshes can strongly benefit from excluding herbivores and the introduction of reed, and that otherwise other vegetation types may establish more slowly in newly created wetlands. This illustrates how active management of vegetation development has the potential to benefit novel ecosystems.

The restoration of degraded ecosystems and landscapes is challenging, because returning to the original state is often socio-economically unfeasible. A novel approach is to construct new ecosystems to improve the functioning of degraded landscapes. However, the development of novel ecosystems is largely driven by the pre-construction hydrogeophysical and ecological conditions of the soil. In Lake Markermeer, a deteriorating freshwater lake in the Netherlands, a large archipelago is currently being constructed to boost the ecological functioning of the lake. Hence, islands – with wetlands and with more elevated and dryer areas – have been created to sustain biodiversity and key biogeochemical functions such as nutrient cycling. The islands are constructed from lake-bottom sediments. To study how two potentially important drivers, water level and bioturbation, affect soil characteristics in a novel wetland ecosystem, we experimentally tested the effects of water level (-30, -10 and 5 cm), and bioturbation by earthworms (Lumbricus rubellus) and Tubifex spp. in a microcosm experiment. We demonstrate that a high water level prevents soil subsidence, soil crack formation and carbon dioxide (CO₂) emissions, and affects nitrogen cycling. In dryer soils, the presence of earthworms strongly increases CO₂ emissions next to reducing soil crack formation, while Tubifex spp. in wetter soils hardly affect soil characteristics. Our findings highlight the important roles of both water level and bioturbation for the functioning of novel soils, which likely affects vegetation development in novel ecosystems. This knowledge can be used to aid the construction and nature development of novel wetlands.

Tropical rainforests are populated by large frugivores that feed upon fruit-producing woody species, yet their role in regulating the cycle of globally important biogeochemical elements such as nitrogen is still unknown. This is particularly relevant because tropical forests play a prominent role in the nitrogen cycle and are becoming rapidly defaunated. Furthermore, frugivory is not considered in current plant-large herbivore-nutrient cycling frameworks exclusively focused on grazers and browsers. Here we used a long-term replicated paired control-exclusion experiment in the Atlantic Forest of Brazil, where peccaries and tapirs are the largest native frugivores, to examine the impact of large ground-dwelling frugivores on modulating soil nitrogen cycling, considering their effects across a gradient of abundance of a hyper-dominant palm. We found that both large frugivores and dominant palms play a substantial role in modulating ammonium availability and nitrification rates. Large frugivores increased ammonium by 95%, which also increased additively with palm abundance. Nitrification rates increased with palm abundance in the presence of large frugivores, but not on exclosure plots. Large frugivores also stimulated the regulation of the functions of soil-nitrifying microorganisms, and modulated the landscape-scale variance in nitrogen availability. Such joint effects of large frugivores and palms are consistent with the notion of ‘fruiting lawns’. Our study indicates that frugivory plays a pivotal role in zoogeochemistry in tropical forests by regulating and structuring the nitrogen cycle, urging to accommodate frugivory in plant-large herbivore-nutrient cycling frameworks. It also indicates that defaunation, deforestation and illegal palm and timber harvesting seriously affect nitrogen cycling in tropical forests, that play a prominent role in the global cycle of this nutrient. A free Plain Language Summary can be found within the Supporting Information of this article.

Land abandonment has been increasing in recent decades in Europe, usually accompanied by biodiversity decline. Whether livestock grazing and mowing can safeguard biodiversity across spatial scales in the long term is unclear. Using a 48-year experiment in a salt marsh, we compared land abandonment (without grazing and mowing) and seven management regimes including cattle grazing, early season mowing, late season mowing, both early and late season mowing, and grazing plus each of the mowing regimes on plant diversity at the local and larger scales (i.e. aggregated local communities). Also, we compared their effects on community composition (both in identities and abundances) in time and space. Under land abandonment, plant diversity declined in the local communities and this decline became more apparent at the larger scale, particularly for graminoids and halophytes. All management regimes, except for late season mowing, maintained plant diversity at these scales. Local plant communities under all treatments underwent different successional trajectories, in the end, diverged from their initial state except for that under grazing (a cyclic succession). Year-to-year changes in local community composition remained at a similar level over time under land abandonment and grazing plus early season mowing while it changed under other treatments. Vegetation homogenized at the larger scale over time under land abandonment while vegetation remained heterogeneous under all management regimes. Synthesis. Our experiment suggests that late season mowing may not be sustainable to conserve plant diversity in salt marshes. Other management regimes can maintain plant diversity across spatial scales and vegetation heterogeneity at the larger scale in the long term, but local community composition may change over time.

Aquatic plants are vital components of shallow aquatic ecosystems, and they can substantially contribute to food webs. However, the large spatial and temporal variations of δ¹³C and δ¹⁵N signatures of aquatic plants have hindered the interpretation of their trophic interactions with organisms at higher trophic levels, and the effects of temperature on plant isotopic signatures remain to be fully elucidated. Herein, we cultured three common submerged macrophytes [Elodea nuttallii (Planch.) St. John, Vallisneria spiralis L., and Potamogeton lucens L.] at four temperatures (10, 15, 20 and 25 °C) for 16 weeks and analyzed their δ¹³C and δ¹⁵N signatures. Results showed that temperature altered the isotopic signatures of all three plant species. δ¹³C and δ¹⁵N varied by 16.06‰ and 11.68‰ in P. lucens at different temperatures, respectively. Plant δ¹⁵N significantly decreased with rising temperature in all three plant species and was correlated with plant growth, N content, and pore water dissolved inorganic N (DIN) concentrations. Conversely, δ¹³C responded non-linearly with temperature: a hump-shaped response of δ¹³C with temperature was observed for P. lucens. Plant δ¹³C was not correlated with any of the measured parameters. Temperature can alter plant metabolism and photosynthesis and the compositions and concentrations of C and N sources, thereby influencing plant δ¹³C and δ¹⁵N signatures, respectively. Temperature plays a key role in altering plant C and N isotopic signatures. Therefore, we recommend future studies to carefully consider the effects of temperature on plant stable isotopic signatures when interpreting the food contribution of aquatic plants in food webs and long-term environmental changes via historical isotopic signatures of plants exposed to different temperatures, particularly in light of changing climate conditions.

Climate extremes are expected to become more commonplace and more severe, putting species and ecosystems at unprecedented risks. We recommend that rewilding programs can create conditions for ecosystems to endure and recover rapidly from climate extremes by incorporating ecosystem engineers of various body sizes and life forms.

Herbivores alter plant biodiversity (species richness) in many of the world's ecosystems, but the magnitude and the direction of herbivore effects on biodiversity vary widely within and among ecosystems. One current theory predicts that herbivores enhance plant biodiversity at high productivity but have the opposite effect at low productivity. Yet, empirical support for the importance of site productivity as a mediator of these herbivore impacts is equivocal. Here, we synthesize data from 252 large-herbivore exclusion studies, spanning a 20-fold range in site productivity, to test an alternative hypothesis-that herbivore-induced changes in the competitive environment determine the response of plant biodiversity to herbivory irrespective of productivity. Under this hypothesis, when herbivores reduce the abundance (biomass, cover) of dominant species (for example, because the dominant plant is palatable), additional resources become available to support new species, thereby increasing biodiversity. By contrast, if herbivores promote high dominance by increasing the abundance of herbivory-resistant, unpalatable species, then resource availability for other species decreases reducing biodiversity. We show that herbivore-induced change in dominance, independent of site productivity or precipitation (a proxy for productivity), is the best predictor of herbivore effects on biodiversity in grassland and savannah sites. Given that most herbaceous ecosystems are dominated by one or a few species, altering the competitive environment via herbivores or by other means may be an effective strategy for conserving biodiversity in grasslands and savannahs globally.