Liesbeth Bakker

Prof. dr. Liesbeth Bakker

Senior Researcher


Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands



I hope to contribute to the UN Decade of Ecosystem Restoration (2021-2030) by studying the opportunities and impacts of ecosystem restoration by rewilding: providing more room for natural processes.


I study rewilding as a novel ecosystem restoration technique. World-wide steep declines in biodiversity call for large-scale ecosystem restoration. Rewilding is an ecosystem restoration technique aiming to provide more room for natural processes to steer biodiversity recovery as much as possible. Rewilding involves the restoration of water and wind dynamics and reconnection of terrestrial, freshwater and marine habitats as well as the promotion of wildlife by reducing or stopping management and re-introducing key missing engineering native species. In my work, I study the outcomes of rewilding for wildlife, biodiversity and ecosystem services as well as the effect of wildlife itself on ecosystem restoration.

Marker Wadden
Liesbeth Bakker
Rewilding lakes by connecting land and water through wetland development. I study the effect on aquatic food webs, nutrient cycling and biodiversity. Here Marker Wadden, one of the study sites in the Markermeer area.
Sayaguesa cattle on Planken Wambuis
Annika Vermaat
Rewilding by (re-)introduction of large herbivores in grasslands. I study their impact on grassland ecosystems: landscape structure, nutrient cycling and biodiversity. Here, Sayaguesa cattle on our study site Planken Wambuis in the Veluwe area.




  • 2015–Present
    Senior Researcher Netherlands Institute of Ecology
  • 2020–Present
    Professor Rewilding Ecology Wageningen University
  • 2009–2015
    Tenure Track Netherlands Institute of Ecology
  • 2007–2009
    VENI Postdoc Netherlands Institute of Ecology
  • 2005–2007
    Postdoc Netherlands Institute of Ecology
  • 2004–2005
    Postdoc University of Alberta Canada
  • 2003–2004
    Postdoc University of Nebraska USA


  • 1997–2003
    PhD Wageningen University Netherlands
  • 1991–1997
    BSc and MSc University of Groningen Netherlands



Peer-reviewed publicaties

  • Science of the Total Environment

    Water level drawdown induces a legacy effect on the seed bank and retains sediment chemistry in a eutrophic clay wetland

    Kerstin Bouma, (Liesbeth) E.S. Bakker, Marleen Wilborts, Bjorn J.M. Robroek, Leon P. M. Lamers, Perry Cornelissen, Mennobart R. van Eerden, Ralph J.M. Temmink
    The lack of extreme water level fluctuations in managed, non-peat forming wetland ecosystems can result in decreased productivity through the loss of heterogeneity of these ecosystems. Stochastic disruption, such as a water level drawdown, can effectively reverse this effect and return the wetland to a more productive state, associated with higher biodiversity through new vegetation development. Yet, aside from the effect on vegetation dynamics, little is known about longer-term effects (30 years) of a water level drawdown, hereafter referred to as legacy effects, and how this may impact future water level drawdowns.

    Here, we aim to unravel the legacy effects of a water level drawdown, stand alone and along a water level gradient, on seed bank properties and nutrient availability in a eutrophic clay wetland. To identify these, we studied the hydrologically managed nature reserve Oostvaardersplassen in the Netherlands. Here, one section was subjected to a multi-year water level drawdown and another section was kept inundated. We determined seed bank properties in both areas, spatially and along a soil elevation gradient (20 cm). Nutrient availability was measured by taking sediment samples along the water level gradient and through experimental manipulation of the water level in an indoor mesocosm experiment.

    Germination was higher in locations with a water level drawdown history, especially at relatively high elevations. Additionally, the proportion of pioneer species in the seed bank was higher in the water level drawdown area. Overall, nutrient concentrations were higher compared to other aquatic systems. Nutrient availability was higher in the inundated area and did not respond to the water level gradient. We conclude that 30 years after an induced water level drawdown there is no depletion of nutrients, while we still observe a legacy effect in the number of viable seeds in the seed bank.
  • Oikos

    Vertebrate grazing can mitigateimpacts of nutrient addition on plant diversity and insect abundance in a semi-natural grassland

    Ciska Veen, Annika T. Vermaat, Judith Sitters, (Liesbeth) E.S. Bakker

    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.
  • One Earth

    Tree cover and its heterogeneity in natural ecosystems is linked to large herbivore biomass globally

    Lanhui Wang, Joris P.G.M. Cromsigt, Robert Buitenwerf, Erick J. Lundgren, Wang Li, (Liesbeth) E.S. Bakker, Jens-Christian Svenning
    Addressing intertwined crises of climate change and biodiversity loss is a pressing global challenge, with trees playing pivotal roles in promoting carbon sequestration and habitat diversity. However, there is a distinct knowledge gap concerning the global drivers shaping tree cover and its heterogeneity, particularly the roles and relative importance of large herbivores and fire compared to climatic and topo-edaphic conditions. Here, we deploy satellite observations of strictly protected areas worldwide to reveal that in regions where vegetation may be in disequilibrium with climate, high biomass of large herbivores, especially browsers, is inversely related to tree cover but positively associated with its spatial heterogeneity. Conversely, fire reduces both tree cover and heterogeneity. These results suggest that top-down megafauna effects on landscape-scale vegetation openness and heterogeneity manifest worldwide. Our finding supports the need to consider megafauna, particularly large herbivores, in ecosystem effects on climate change mitigation and conservation and restoration efforts through trophic rewilding.
  • Science of the Total Environment

    Creating new littoral zones in a shallow lake to forward-restore an aquatic food web

    Casper van Leeuwen, J. De Leeuw, Joey J.J. Volwater, Olvin A. van Keeken, Hui Jin, Annemieke M. Drost, Dennis Waasdorp, Erik Reichman, L. Ursem, (Liesbeth) E.S. Bakker
    Current rates of habitat loss require science-based predictions on how to restore or newly create lost habitat types. In aquatic ecosystems, littoral zones are key habitats for food web functioning, but they are often replaced by unnatural steep shorelines for water safety. To reverse this trend, knowledge is needed on how to successfully (re)create littoral zones. We quantified the response of an aquatic food web to the large-scale creation of new heterogeneous littoral habitats in shallow lake Markermeer, the Netherlands. Lake Markermeer was formed by dike construction in a former estuary, which created a heavily modified homogeneous 70,000 ha turbid lake lacking littoral habitat. Fish and bird populations declined over the last decades, but classical restoration via return to former marine conditions would compromise water safety and the large spatial scale prohibited biodiversity offsets. Therefore, an innovative “forward-looking restoration” approach was adopted: a 1000 ha archipelago called “Marker Wadden” was constructed without using a historic reference situation to return to. This aimed bottom-up stimulation of the aquatic food web by added missing gradual land-water transitions and sheltered waters to the lake. After four years, new sheltered shorelines had become vegetated if they were constructed from nutrient-rich sediments. Exposed and sandy shorelines remained free of vegetation. Zooplankton community diversity increased in sheltered waters due to bottom-up processes, which increased food availability for higher trophic levels, including young fish. The creation of sheltered waters increased macroinvertebrate densities threefold, with sediment type determining the community composition. The archipelago became new nursery habitat for 13 of the 24 fish species known to occur in the lake, with up to 10-fold higher abundances under sheltered conditions. We conclude that modifying abiotic conditions can stimulate multiple trophic levels in aquatic food webs simultaneously, even in heavily modified ecosystems. This provides proof-of-principle for the forward-looking restoration approach.
  • Movement Ecology

    Multispecies fish tracking across newly created shallow and deep habitats in a forward-restored lake

    Casper van Leeuwen, Joep J. de Leeuw, Olvin A. van Keeken, Joey J.J. Volwater, Ferdi Seljee, Roland van Aalderen, Willie A. M. van Emmerik, (Liesbeth) E.S. Bakker

    Freshwater fish communities typically thrive in heterogenous ecosystems that offer various abiotic conditions. However, human impact increasingly leads to loss of this natural heterogeneity and its associated rich fish communities. To reverse this trend, we need guidelines on how to effectively restore or recreate habitats for multiple fish species. Lake Markermeer in the Netherlands is a human-created 70,000-ha lake with a uniform 4 m-water depth, steep shorelines, high wind-induced turbidity, and a declining fish community. In 2016, a forward-looking restoration project newly created a 1000-ha five-island archipelago in this degrading lake, which offered new sheltered shallow waters and deep sand excavations to the fish community.

    In 2020, we assessed how omnivorous and piscivorous fish species used these new habitats by tracking 78 adult fish of five key species across local and lake-scales. We monitored spring arrival of adult fish and assessed local macro-invertebrate and young-of-the-year fish densities.

    Adult omnivorous Cyprinidae and piscivorous Percidae arrived at the archipelago in early spring, corresponding with expected spawning movements. During the productive summer season, 12 species of young-of-the-year fish appeared along the sheltered shorelines, with particularly high densities of common roach (Rutilus rutilus) and European perch (Perca fluviatilis). This suggests the sheltered, shallow, vegetated waters formed new suitable spawning and recruitment habitat for the fish community. Despite highest food densities for adult fish in the shallowest habitats (Conclusions

    New littoral zones and a deep sand excavation constructed in a uniform shallow lake that lacked these habitat types attracted omnivorous and piscivorous fish species within four years. Both feeding guilds used the littoral zones for reproduction and nursery, and notably piscivorous fish became residents year-round.
  • Journal of Ecology

    Large mammalian herbivores affect arthropod food webs via changes in vegetation characteristics and microclimate

    Yu Zhu, Ciska Veen, Robin Heinen, Deli Wang, Ming Jiang, Hui Jin, (Liesbeth) E.S. Bakker
    Large mammalian herbivores are vital components of terrestrial ecosystems, influencing the plants they feed on, but also serving as ecosystem engineers that impact the occurrence and survival of many other organisms. Arthropods are the most abundant and diverse animal group on earth, filling all trophic levels in food webs and facilitating essential ecosystem services. However, the impacts of large herbivores on arthropod communities and the mechanisms via which these impacts are mediated are not fully understood.
    Here, we experimentally separated the mechanistic pathways whereby large herbivores affect arthropod food webs using a 24-year manipulative multi-site field experiment in the Netherlands. We analysed the abundance, biomass and community composition of arthropods in the plant canopy and on the soil surface, both in grazed sites or sites where large herbivores were excluded.
    We found that the presence of large herbivores resulted in considerable differences in vegetation properties and microclimate which influenced the abundance and biomass of arthropods to varying trophic levels. Large herbivore grazing enhanced the overall abundance and biomass of arthropod herbivores, pollinators, omnivores and soil-dwelling predators, but reduced that of detritivores, scavengers, parasitoids and canopy predators. Structural equation models revealed that different trophic groups are affected by grazing via different pathways. Specially, large herbivores facilitated herbivores via increasing plant quality and enhanced ground-dwelling predators via increasing plant diversity. In contrast, plant-dwelling predators were suppressed via decreased plant quantity, and parasitoids were mainly affected by changes in microclimate conditions.
    Synthesis. Our results show that large mammalian herbivores play a significant role in shaping grassland arthropod food webs, and that these impacts were independently mediated by multiple aspects of vegetation properties, that is, physical structure, plant diversity, standing crop biomass and leaf nutrient content. Arthropods of different trophic groups responded differently to the large herbivores, and these functional group-specific responses in turn may have strong cascading effects on numerous ecosystem services.
  • Water Research

    Restoring gradual land-water transitions in a shallow lake improved phytoplankton quantity and quality with cascading effects on zooplankton production

    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.
  • Nature Climate Change

    Trophic rewilding can expand natural climate solutions

    Oswald J. Schmitz, Magnus Sylvén, Trisha B. Atwood, (Liesbeth) E.S. Bakker, Fabio Berzaghi, Jedediah F. Brodie, Joris P.G.M. Cromsigt, Andrew B. Davies, Shawn J. Leroux, Frans J. Schepers, Felisa A. Smith, Sari Stark, Jens-Christian Svenning, Andrew Tilker, Henni Ylänne
    Natural climate solutions are being advanced to arrest climate warming by protecting and enhancing carbon capture and storage in plants, soils and sediments in ecosystems. These solutions are viewed as having the ancillary benefit of protecting habitats and landscapes to conserve animal species diversity. However, this reasoning undervalues the role animals play in controlling the carbon cycle. We present scientific evidence showing that protecting and restoring wild animals and their functional roles can enhance natural carbon capture and storage. We call for new thinking that includes the restoration and conservation of wild animals and their ecosystem roles as a key component of natural climate solutions that can enhance the ability to prevent climate warming beyond 1.5 °C.
  • Ecological Entomology

    Contrasting effects of nitrogen fertiliser application on the performance of closely related grasshoppers through changes in plant nutrient concentrations

    Yu Zhu, Quanhui Ma, Zhiwei Zhong, Ming Jiang, (Liesbeth) E.S. Bakker, Jeff A. Harvey, Ciska Veen, Cong Chen, Deli Wang
    Global environmental changes mediated by anthropogenic processes can affect the nutrient status of plants, with important consequences for the performance and dynamics of insect herbivores that feed on them.
    While it is well documented that insects from different feeding guilds (e.g., sap-feeders and leaf-chewers) can respond differently to altered food resources due to their distinct physiological and ecological characteristics, little is known about how ecologically similar insect species from the same feeding guild respond to changes in food nutrient status.
    Using nitrogen (N) fertiliser, the authors examined the effects of N inputs on two sympatric grasshopper species, Euchorthippus cheui and E. unicolor, that share the same host food plant, Leymus chinensis grass. The authors examined the effects of fertilisation on the individual feeding behaviour, performance and abundance of the two grasshopper species.
    The nutrient (protein) content of L. chinensis leaves was enhanced by fertilisation during the entire season. However, E. cheui and E. unicolor exhibited differing growth rates, development and body size responses to fertilisation.
    E. cheui preferred L. chinensis leaves from high-N fertilised treatments, while E. unicolor preferred leaves from low-N fertilised treatments. Moreover, fertilisation increased the abundance of E. cheui but had no significant effect on the abundance of E. unicolor in the field.
    The findings imply that effective management and conservation strategies for insects should target the needs of individual species rather than species groups or communities as a whole because nutritional and environmental requirements are often species-specific.
  • Ecography

    Seed dispersal by waterbirds: a mechanistic understanding by simulating avian digestion

    Casper van Leeuwen, Merel Soons, Laura Vandionant, Andy J. Green, (Liesbeth) E.S. Bakker
    Waterbirds disperse plant species via ingestion and egestion of seeds (endozoochory). However, our understanding about the regulating effects of seed traits, underlying mechanisms and possible (co)evolutionary processes is limited by our traditional reliance on data from feeding experiments with living waterbirds. Here, we overcome these limitations by developing and applying a new bioassay that realistically simulates digestive processes for Anseriformes waterbirds. We test three hypotheses: 1) seed survival and germination are most affected by mechanical digestion in the waterbird gizzard; 2) seed size, hardness, imbibition and shape regulate seed survival; and 3) plants growing in aquatic habitats benefit most from endozoochory by waterbirds. Experiments with 28 200 seeds of 48 plant species demonstrated species-specific seed survival that was entirely determined by digestion in the avian gizzard. Intestinal digestion did not affect seed survival but affected seed establishment (germinability and germination time) for 21% of the species. Large, hard seeds survived the simulations the best, in contrast to generally higher seed survival for smaller seeds during in vivo experiments. This mechanistically explains that small seeds escape digestive processes rather than being inherently more resistant (the ‘escape mechanism'), while large seeds are retained until fully digested or regurgitated (the ‘resistance and regurgitation mechanism'). Plants growing in wetter habitats had similar seed survival, but digestive processes stimulated their germinability and accelerated their germination more than for terrestrial plants. This indicates a relative advantage of endozoochory for plant species growing in wet habitats, possibly reflecting a co-evolutionary response related to dormancy breaking by gut passage. Simulating seed gut passage using a bioassay allowed establishing mechanisms and identifying relevant seed traits involved in seed dispersal by waterbirds. This information enhances our understanding of how animal species shape plant species distributions, which is extremely relevant now that current anthropogenic pressures already severely impact plant dispersal capacities.
  • Landschap

    Moerasontwikkeling op voormalige landbouwgrond

    Jimmy De Fouw, Ron van der Hut, Alfons J. P. Smolders, Jan van der Winden, (Liesbeth) E.S. Bakker, Piet-Jan Westendorp
  • Aquatic Botany

    Fish grazing enhanced by nutrient enrichment may limit invasive seagrass expansion

    Fee O.H. Smulders, S. Tatiana Becker, Justin E. Campbell, (Liesbeth) E.S. Bakker, Mickey J. Boässon, Mark M. Bouwmeester, J. Arie Vonk, Marjolijn J.A. Christianen

    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.
  • Aquatic Botany

    Submerged vegetation colonizes behind artificial wave shelter after a 10-year time-lag and persists under high grazing pressure by waterbirds

    Bastiaan G. van Zuidam, (Liesbeth) E.S. Bakker, G.J. Van Geest, Edwin T.H.M. Peeters

    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.
  • Science of the Total Environment

    Impacts of sediment resuspension on phytoplankton biomass production and trophic transfer: Implications for shallow lake restoration

    Wind-induced sediment resuspension in shallow lakes may enhance nutrient availability while reducing light availability for phytoplankton growth, thereby affecting the entire food-web. Lake restoration projects that reduce wind-induced resuspension are expected to enhance trophic transfer efficiencies, thereby improving food-web structure and functioning. Yet, reduced resuspension may also lead to lower nutrient concentrations in the water column, promote benthic algae development, reduce phytoplankton biomass production and thereby reduce secondary production by zooplankton. Lake Markermeer is a shallow delta lake in The Netherlands subject to wind-induced sediment resuspension. Restoration project Marker Wadden consists of newly built islands aiming to reduce sediment resuspension and promote higher trophic levels. Here, we tested the effects of reduced sediment resuspension on phytoplankton biomass build-up, benthic algae development, and zooplankton abundances at different temperatures in a 14-day indoor microcosm experiment. We used Marker Wadden sediment with three resuspension intensities combined with three temperatures, to also test effects of higher temperatures in shallow sheltered waters. Reduced sediment resuspension decreased nutrient concentrations and phytoplankton biomass build-up, while increasing light availability and enhancing benthic algae biomass development. Reduced sediment resuspension furthermore increased zooplankton biomass. Enhanced sediment resuspension and higher temperatures synergistically interacted, maintaining a high level of inorganic suspended solids. Our experimental results are in line with long-term seasonal observations from Lake Markermeer. Our findings demonstrate that for shallow lakes suffering from wind effects, measures such as Marker Wadden aimed at reducing sediment resuspension can be effective in restoring secondary production and supporting higher trophic levels.
  • Limnology and Oceanography

    Differential effects of elevated pCO2 and warming on marine phytoplankton stoichiometry

    Mandy Velthuis, Joost Keuskamp, (Liesbeth) E.S. Bakker, Maarten Boersma, U. Sommer, Ellen Van Donk, Dedmer Van de Waal
    Phytoplankton stand at the base of the marine food-web, and play a major role in global carbon cycling. Rising CO2 levels and temperatures are expected to enhance growth and alter carbon:nutrient stoichiometry of marine phytoplankton, with possible consequences for the functioning of marine food-webs and the oceanic carbon pump. To date, however, the consistency of phytoplankton stoichiometric responses remains unclear. We therefore performed a meta-analysis on data from experimental studies on stoichiometric responses of marine phytoplankton to elevated pCO2 and 3–5° warming under nutrient replete and limited conditions. Our results demonstrate that elevated pCO2 increased overall phytoplankton C:N (by 4%) and C:P (by 9%) molar ratios under nutrient replete conditions, as well as phytoplankton growth rates (by 6%). Nutrient limitation amplified the CO2 effect on C:N and C:P ratios, with increases to 27% and 17%, respectively. In contrast to elevated pCO2, warming did not consistently alter phytoplankton elemental composition. This could be attributed to species- and study-specific increases and decreases in stoichiometry in response to warming. While our observed moderate CO2-driven changes in stoichiometry are not likely to drive marked changes in food web functioning, they are in the same order of magnitude as current and projected estimations of oceanic carbon export. Therefore, our results may indicate a stoichiometric compensation mechanism for reduced oceanic carbon export due to declining primary production in the near future.
  • Ecological Engineering

    Herbivore exclusion and active planting stimulate reed marsh development on a newly constructed archipelago

    Ralph J.M. Temmink, Marloes van den Akker, Casper van Leeuwen, Yvonne Thöle, Han Olff, Valerie Reijers, Stefan T.J. Weideveld, Bjorn J.M. Robroek, Leon P. M. Lamers, (Liesbeth) E.S. Bakker

    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.
  • Ecology

    Green turtles shape the seascape through grazing patch formation around habitat features

    Fee O.H. Smulders, (Liesbeth) E.S. Bakker, O. R. O'Shea, Justin E. Campbell, O. K. Rhoades, M.J.A. Christianen

    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.
  • Oikos

    A Seed Dispersal Effectiveness framework across the mutualism-antagonism continuum

    Casper van Leeuwen, Nacho Villar, I. Mendoza-Sagrera, Andy J. Green, (Liesbeth) E.S. Bakker, Merel Soons, Mauro Galetti, Patrick A. Jansen, Bart A. Nolet, Luis Santamaría
    Many angiosperms rely on vertebrates for seed dispersal via gut passage, an interaction that has been traditionally classified as a mutualism. The seed dispersal effectiveness (SDE) framework provides a mechanistic approach to evaluate evolutionary and ecological characteristics of animal-mediated seed dispersal, by synthesising the quantity and the quality of the dispersal that a plant species receives from each of its animal dispersers. However, the application of the SDE framework has been largely restricted to plant–frugivore interactions, whereas animal-mediated seed dispersal results from plant–disperser interactions that cover a continuum from pure mutualisms to antagonisms. This biases ecological and evolutionary knowledge on plant–disperser interactions. Here, we propose an extended SDE framework (‘eSDE') that allows comparing plant–disperser interactions in the full mutualism–antagonism continuum ranging from pure mutualisms (frugivores) to conditional mutualisms (scatter-hoarding granivores and folivores) and antagonisms (pure granivores). We present the eSDE framework, and use examples to illustrate how it can be applied to compare effectiveness among plant–disperser interaction types. Our initial comparison based on available data suggests that vertebrate species differ more in the number of seeds they deposit away from the mother plant (quantity), than in the effects such dispersal processes have on seed fate (quality). Scatter-hoarding granivores provide the most effective dispersal due to high removal rates, closely followed by frugivores due to high deposition rates. Folivores and pure granivores provide low quantity dispersal, but of high and moderate quality, respectively. These early comparative insights illustrate the necessity and usefulness of more standardized data collection protocols, for which we provide recommendations. Applying the eSDE framework can reveal broad-scale patterns across and within plant–disperser interaction types, which will advance our evolutionary understanding of plant–animal interactions. This will provide new insights into the consequence of anthropogenic impacts on vertebrate-mediated seed dispersal in a world in which plant–animal interactions are increasingly threatened.
  • Nature Ecology and Evolution

    Evolutionary history of grazing and resources determine herbivore exclusion effects on plant diversity

    Jodi N. Price, Judith Sitters, Timothy J. Ohlert, Pedro M. Tognetti, Cynthia S. Brown, Eric W. Seabloom, Elizabeth T. Borer, Suzanne M. Prober, (Liesbeth) E.S. Bakker, Andrew S. MacDougall, Laura Yahdjian, Daniel S. Gruner, Harry Olde Venterink, Isabel C. Barrio, Pamela Graff, Sumanta Bagchi, Carlos Alberto Arnillas, Jonathan D. Bakker, Dana M. Blumenthal, Elizabeth H Boughton, Lars A. Brudvig, Miguel N. Bugalho, Marc W. Cadotte, Maria C. Caldeira, Chris R. Dickman, Ian Donohue, Sonnier Grégory, Yann Hautier, I.S. Jonsdottir, Lucíola S. Lannes, Rebecca L. McCulley, Joslin L. Moore, Sally A. Power, Anita C. Risch, Martin Schütz, Rachel Standish, Carly J. Stevens, Ciska Veen, Risto Virtanen, Glenda M. Wardle

    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.
  • Freshwater Biology

    Impacts of shelter on the relative dominance of primary producers and trophic transfer efficiency in aquatic food webs

    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.
  • Global Change Biology

    Seagrass ecosystem multifunctionality under the rise of a flagship marine megaherbivore

    Marjolijn J.A. Christianen, Fee O.H. Smulders, J. Arie Vonk, Leontine E. Becking, T.J. Bouma, Sabine M. Engel, Rebecca K. James, Mabel I. Nava, Jaco C. de Smit, Jurjan P. van der Zee, Per J. Palsbøll, (Liesbeth) E.S. Bakker
    Large grazers (megaherbivores) have a profound impact on ecosystem functioning. However, how ecosystem multifunctionality is affected by changes in megaherbivore populations remains poorly understood. Understanding the total impact on ecosystem multifunctionality requires an integrative ecosystem approach, which is especially challenging to obtain in marine systems. We assessed the effects of experimentally simulated grazing intensity scenarios on ecosystem functions and multifunctionality in a tropical Caribbean seagrass ecosystem. As a model, we selected a key marine megaherbivore, the green turtle, whose ecological role is rapidly unfolding in numerous foraging areas where populations are recovering through conservation after centuries of decline, with an increase in recorded overgrazing episodes. To quantify the effects, we employed a novel integrated index of seagrass ecosystem multifunctionality based upon multiple, well-recognized measures of seagrass ecosystem functions that reflect ecosystem services. Experiments revealed that intermediate turtle grazing resulted in the highest rates of nutrient cycling and carbon storage, while sediment stabilization, decomposition rates, epifauna richness, and fish biomass are highest in the absence of turtle grazing. In contrast, intense grazing resulted in disproportionally large effects on ecosystem functions and a collapse of multifunctionality. These results imply that (i) the return of a megaherbivore can exert strong effects on coastal ecosystem functions and multifunctionality, (ii) conservation efforts that are skewed toward megaherbivores, but ignore their key drivers like predators or habitat, will likely result in overgrazing-induced loss of multifunctionality, and (iii) the multifunctionality index shows great potential as a quantitative tool to assess ecosystem performance. Considerable and rapid alterations in megaherbivore abundance (both through extinction and conservation) cause an imbalance in ecosystem functioning and substantially alter or even compromise ecosystem services that help to negate global change effects. An integrative ecosystem approach in environmental management is urgently required to protect and enhance ecosystem multifunctionality.
  • Pedobiologia

    Nature development in degraded landscapes: How pioneer bioturbators and water level control soil subsidence, nutrient chemistry and greenhouse gas emission

    Ralph J.M. Temmink, Marloes van den Akker, Bjorn J.M. Robroek, Peter M.J.M. Cruijsen, Annelies Veraart, Sarian Kosten, Roy C.J.H. Peters, Germa M. Verheggen-Kleinheerenbrink, Aniek W. Roelofs, Xiomara van Eek, (Liesbeth) E.S. Bakker, Leon P. M. Lamers

    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.
  • Functional Ecology

    Frugivory underpins the nitrogen cycle

    Nacho Villar, Claudia Paz, Valesca Zipparro, Sergio Nazareth, Leticia Bulascoschi, (Liesbeth) E.S. Bakker, Mauro Galetti

    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.
  • Journal of Ecology

    Long-term cross-scale comparison of grazing and mowing on plant diversity and community composition in a salt-marsh system

    Qingqing Chen, Jan P. Bakker, Juan Alberti, (Liesbeth) E.S. Bakker, Christian Smit, Han Olff

    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 Sciences

    Temperature affects carbon and nitrogen stable isotopic signatures of aquatic plants

    Peiyu Zhang, Xianghong Kong, (Liesbeth) E.S. Bakker, Jun Xu, Min Zhang

    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.
  • Ecological Solutions and Evidence

    Enhancing ecological integrity while preserving ecosystem services: constructing soft-sediment islands in a shallow lake

    Casper van Leeuwen, Ralph J.M. Temmink, Hui Jin, Y Kahlert, B.J.M. Robroek, M.P. Berg, Leon P. M. Lamers, Marloes van den Akker, R. Posthoorn, A. Boosten, Han Olff, (Liesbeth) E.S. Bakker
    Abstract Ecosystems are increasingly managed to provide multiple benefits to humans, which often degrades their ecological integrity. This strongly applies to aquatic ecosystems, in which engineering can enhance flood protection, drinking water supply, fisheries and recreation. Although these activities typically increase ecosystem functionality to humans, they often impair key aspects of biodiversity and natural functioning. Classical restoration of such degrading freshwater ecosystems can lead to societal opposition, if returning to a former ecosystem state affects previously acquired ecosystem services. Innovative nature-based solutions are therefore needed that enhance natural values in ecosystems, without affecting existing services. We present a large-scale project aiming to increase the ecological integrity of a human-modified freshwater lake while maintaining its services to humans. The freshwater lake Markermeer in the Netherlands was formed by closing off an estuary for flood protection. The ecological integrity of this lake diminished over time, likely because a declining primary productivity impaired biodiversity at higher trophic levels. This decline is associated with a lack of gradual land?water transitions, strong resuspension of fine sediments, low nutrient availability and lack of dynamics typically to be expected in a natural temperate freshwater lake. Restoring the lake to its former marine state would conflict with current ecosystem services. A nature-based solution was initiated in 2016, consisting of constructing a five-island archipelago from the lake's own soft-sediments called the ?Marker Wadden?. The project aims to increase the lake's primary production by creating gradual land?water transitions, more heterogeneity in water depths and decreasing turbidity by creating shelter and deep sinks reducing fine-sediment resuspension by the wind ? thus introducing currently missing elements that are typical for natural lakes. We present the underlying ecological framework and first scientific results of this innovative ongoing project. Within 4 years, the Marker Wadden project shows how forward-looking sustainable development of lake ecosystems using a rewilding approach can enhance natural processes and attract birds and fish, without conflicting with existing ecosystem services. This inspires new directions for halting and reversing the degradation of other vital ecosystems worldwide.
  • Journal of Ecology

    Seagrass coastal protection services reduced by invasive species expansion and megaherbivore grazing

    Rebecca K. James, Marjolijn J.A. Christianen, Marieke M. van Katwijk, Jaco C. de Smit, (Liesbeth) E.S. Bakker, Peter M.J. Herman, T.J. Bouma
    Abstract Seagrasses provide an important ecosystem service by creating a stable erosion-resistant seabed that contributes to effective coastal protection. Variable morphologies and life-history strategies, however, are likely to impact the sediment stabilization capacity of different seagrass species. We question how opportunistic invasive species and increasing grazing by megaherbivores may alter sediment stabilization services provided by established seagrass meadows, using the Caribbean as a case study. Utilizing two portable field-flumes that simulate unidirectional and oscillatory flow regimes, we compared the sediment stabilization capacity of natural seagrass meadows in situ under current- and wave-dominated regimes. Monospecific patches of a native (Thalassia testudinum) and an invasive (Halophila stipulacea) seagrass species were compared, along with the effect of three levels of megaherbivore grazing on T. testudinum: ungrazed, lightly grazed and intensively grazed. For both hydrodynamic regimes, the long-leaved, dense meadows of the climax species, T. testudinum provided the highest stabilization. However, the loss of above-ground biomass by intensive grazing reduced the capacity of the native seagrass to stabilize the surface sediment. Caribbean seagrass meadows are presently threatened by the rapid spread of the invasive opportunistic seagrass, H. stipulacea. The dense meadows of H. stipulacea were found to accumulate fine sediment, and thereby, appear to be effective in reducing bottom shear stress during calm periods. This fine sediment within the invasive meadows, however, is easily resuspended by hydrodynamic forces, and the low below-ground biomass of H. stipulacea make it susceptible to uprooting during storm events, potentially leaving large regions vulnerable to erosion. Overall, this present study highlights that intensive megaherbivore grazing and opportunistic invasive species threaten the coastal protection services provided by mildly grazed native species. Synthesis. Seagrass meadows of dense, long-leaved species stabilize the sediment surface and maintain the seabed integrity, thereby contributing to coastal protection. These services are threatened by intensive megaherbivore grazing, which reduces the stability of the surface sediment, and opportunistic invasive species, which are susceptible to uprooting in storms and thereby can leave the seabed vulnerable to erosion.
  • Oikos

    Ectothermic omnivores increase herbivory in response to rising temperature

    Peiyu Zhang, Casper van Leeuwen, Dagmar Bogers, Marjolein Poelman, Jun Xu, (Liesbeth) E.S. Bakker
    Higher temperatures as a consequence of global climate change may considerably alter trophic interactions. Ectothermic herbivores and carnivores generally ingest more food with rising temperature as their metabolic rates increase with rising temperature. However, omnivorous ectotherms may respond in two ways: quantitatively by consuming more food and qualitatively by altering their degree of herbivory or carnivory through a diet shift. We hypothesize that rising temperature will increase herbivory of ectothermic omnivores as herbivory increases towards the equator. We tested the hypothesis in a freshwater model system in which ectothermic omnivores are prevalent, by applying two approaches, a temperature manipulation experiment and a literature study. We performed feeding trials with a juvenile aquatic ectothermic omnivore (pond snail Lymnaea stagnalis) at different temperatures ranging from 12 to 27°C, supplying them with both animal food and plant material, and directly quantified their consumption rates over time. The results showed that snails cultured at high temperatures (> 21°C) increased the proportion of plant material in their diets after 17 days, which supports our hypothesis. In the literature survey, we found that rising temperature increased herbivory in multiple aquatic animal taxa, including zooplankton, amphibians, crayfish, fish and snails. This suggests that aquatic ectothermic omnivores might commonly increase herbivory with rising temperature. The mechanisms underlying this temperature‐induced diet shift are not sufficiently explained by current theories related to the physiology, metabolism and stoichiometry of omnivores. We propose to incorporate the animals’ ontogenetic development in the temperature metabolic stoichiometry hypothesis as a complementary explanation for the diet shift, namely that the diet shift could be due to faster development of the ectotherms and an earlier ontogenetic diet shift at higher temperatures. We conclude that future global warming will most likely alter food webs by increasing the top–down control of aquatic herbivores and omnivores on primary producers.
  • Journal of Ecology

    Direct and indirect effects of native plants and herbivores on biotic resistance to alien aquatic plant invasions

    Biotic resistance to alien plant invasions is mainly determined by ecological interactions in two layers of the food web: competition with native plant species and herbivory by native herbivores. While the direct effect of native plants on alien plant performance via competition has been well documented across ecosystems, less is known about the direct and indirect effects of herbivores in providing biotic resistance. Our main aims were to determine whether temperate native aquatic plants and herbivores can provide biotic resistance to plant invasions, understand the underlying mechanisms and search for potential interactive effects of competition and herbivory on invader performance (i.e. growth).
    We mimicked natural temperate mesotrophic and eutrophic freshwater lakes in mesoscosms, by growing three native submerged plant species in monocultures (Ceratophyllum demersum, Myriophyllum spicatum and Potamogeton perfoliatus) at three competition levels (no, low and high) without and with the native aquatic generalist snail Lymnaea stagnalis. We subsequently simulated an early stage of establishment of the South American highly invasive alien plant species Egeria densa.
    We found that competition by native plant biomass significantly reduced invader performance but depended on native species identity. Herbivory had no direct negative effect on invader performance as the snails fed mainly on the available filamentous algae, which are commonly found in meso‐ and eutrophic systems, instead of on the plants. However, the consumption of filamentous algae by herbivores indirectly had positive effects on the invader total biomass, thus facilitating the invasion by E. densa. Nonetheless, these indirect effects worked through different pathways depending on the native plant identity.
    Synthesis. We found evidence for biotic resistance through competition by native plant species. However, we show that herbivores can indirectly facilitate South American plant E. densa invasion promoting its growth through selective feeding on filamentous algae, but this effect depends on the native plant species involved. Our experiment illustrates the important role of indirect interactions to understand the potential of biotic resistance in natural ecosystems.
  • Global Change Biology

    Nutrient availability controls the impact of mammalian herbivores on soil carbon and nitrogen pools in grasslands

    Judith Sitters, Jasper Wubs, (Liesbeth) E.S. Bakker, Tom Crowther, Peter B. Adler, Sumanta Bagchi, Jonathan D. Bakker, Lori A. Biederman, Elizabeth T. Borer, Elsa E. Cleland, Nico Eisenhauer, J Firn, Laureano Gherardi, Nicole Hagenah, Yann Hautier, Sarah Hobbie, Johannes M. H. Knops, A.S. MacDougall, Rebecca L. McCulley, Joslin L. Moore, Brent Mortensen, Pablo L. Peri, Suzanne M. Prober, C Riggs, Anita C. Risch, Martin Schütz, Eric W. Seabloom, Julia Siebert, Carly J. Stevens, Ciska Veen
    Grasslands are subject to considerable alteration due to human activities globally, including widespread changes in populations and composition of large mammalian herbivores and elevated supply of nutrients. Grassland soils remain important reservoirs of carbon (C) and nitrogen (N). Herbivores may affect both C and N pools and these changes likely interact with increases in soil nutrient availability. Given the scale of grassland soil fluxes, such changes can have striking consequences for atmospheric C concentrations and the climate. Here, we use the Nutrient Network experiment to examine the responses of soil C and N pools to mammalian herbivore exclusion across 22 grasslands, under ambient and elevated nutrient availabilities (fertilized with NPK + micronutrients). We show that the impact of herbivore exclusion on soil C and N pools depends on fertilization. Under ambient nutrient conditions, we observed no effect of herbivore exclusion, but under elevated nutrient supply, pools are smaller upon herbivore exclusion. The highest mean soil C and N pools were found in grazed and fertilized plots. The decrease in soil C and N upon herbivore exclusion in combination with fertilization correlated with a decrease in aboveground plant biomass and microbial activity, indicating a reduced storage of organic matter and microbial residues as soil C and N. The response of soil C and N pools to herbivore exclusion was contingent on temperature – herbivores likely cause losses of C and N in colder sites and increases in warmer sites. Additionally, grasslands that contain mammalian herbivores have the potential to sequester more N under increased temperature variability and nutrient enrichment than ungrazed grasslands. Our study highlights the importance of conserving mammalian herbivore populations in grasslands worldwide. We need to incorporate local‐scale herbivory, and its interaction with nutrient enrichment and climate, within global‐scale models to better predict land–atmosphere interactions under future climate change.
  • Aquatic Botany

    On the move: New insights on the ecology and management of native and alien macrophytes

    Deborah E. Hofstra, Jonas Schoelynck, Jason Ferrell, Julie Coetzee, Mary de Winton, Tobias Bickel, Paul Champion, John Madsen, (Liesbeth) E.S. Bakker, Sabine Hilt, Fleur Matheson, Mike Netherland, Elisabeth M. Gross
    Globally, freshwater ecosystems are under threat. The main threats come from catchment land-use changes, altered water regimes, eutrophication, invasive species, climate change and combinations of these factors. We need scientific research to respond to these challenges by providing solutions to halt the deterioration and improve the condition of our valuable freshwaters. This requires a good understanding of aquatic ecosystems, and the nature and scale of changes occurring. Macrophytes play a fundamental role in aquatic systems. They are sensitive indicators of ecosystem health, as they are affected by run-off from agricultural, industrial or urban areas. On the other hand, alien macrophytes are increasingly invading aquatic systems all over the world. Improving our knowledge on the ecology and management of both native and alien plants is indispensable to address threats to freshwaters in order to protect and restore aquatic habitats. The International Aquatic Plants Group (IAPG) brings together scientists and practitioners based at universities, research and environmental organisations around the world. The main themes of the 15th symposium 2018 in New Zealand were biodiversity and conservation, management, invasive species, and ecosystem response and restoration. This Virtual Special Issue provides a comprehensive review from the symposium, addressing the ecology of native macrophytes, including those of conservation concern, and highly invasive alien macrophytes, and the implications of management interventions. In this editorial paper, we highlight insights and paradigms on the ecology and management of native and alien macrophytes gathered during the meeting.
  • Scientific Reports

    Species identity and diversity effects on invasion resistance of tropical freshwater plant communities

    Antonella Petruzzella, Tauany A. da S. S. R. Rodrigues, Casper van Leeuwen, Francisco de Assis Esteves, Marco Paulo Figueiredo-Barros, (Liesbeth) E.S. Bakker
  • One Earth

    Climate Extremes, Rewilding, and the Role of Microhabitats

    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.
  • Oikos

    Herbivore phenology can predict response to changes in plant quality by livestock grazing

    Yu Zhu, Ciska Veen, Deli Wang, Ling Wang, Zhiwei Zhong, Quanhui Ma, Heng Li, Xincheng Li, Duofeng Pan, (Liesbeth) E.S. Bakker
    Livestock grazing can have a strong impact on herbivore abundance, distribution and community. However, not all species of herbivores respond the same way to livestock grazing, and we still have a poor understanding of the underlying mechanisms driving these differential responses. Here, we investigate the effect of light intensity cattle grazing on the abundance of two grasshoppers (Euchorthippus cheui and E. unicolor) that co-occur in the same grasslands and feed on the same food plant (the dominant grass Leymus chinensis). The two grasshopper species differ in phenology so that their peak abundances are separated into early- and late-growing seasons. We used an exclosure experiment to monitor grasshopper abundance and food quality in the field under grazed and ungrazed conditions, and performed feeding trials to examine grasshopper preference for grazed or ungrazed food plants in the laboratory. We found that the nitrogen content of L. chinensis leaves continuously declined in the ungrazed areas, but was significantly enhanced by cattle grazing over the growing season. Cattle grazing facilitated the early-season grasshopper E. cheui, whereas it suppressed the late-season grasshopper E. unicolor. Moreover, feeding trials showed that E. cheui preferred L. chinensis from grazed plots, while E. unicolor preferred the leaves from ungrazed plots. We conclude that livestock grazing has opposite effects on the two grasshopper species, and that these effects may be driven by grazing-induced changes in plant nutrient content and the unique nutritional niches of the grasshoppers. These results suggest that insects that belong to the same guild can have opposite nutrient requirements, related to their distinct phenologies, and that this can ultimately affect their response to cattle grazing. Our results show that phenology may link insect physiological needs to local resource availabilities, and should be given more attention in future work on interactions between large herbivores and insects.
  • Frontiers in Plant Science

    Effects of Rising Temperature on the Growth, Stoichiometry, and Palatability of Aquatic Plants

    Peiyu Zhang, Bart Grutters, Casper van Leeuwen, Jun Xu, Antonella Petruzzella, Reinier van den Berg, (Liesbeth) E.S. Bakker
    Global warming is expected to strengthen herbivore-plant interactions leading to enhanced top-down control of plants. However, latitudinal gradients in plant quality as food for herbivores suggest lower palatability at higher temperatures, but the underlying mechanisms are still unclear. If plant palatability would decline with temperature rise, then this may question the expectation that warming leads to enhanced top-down control. Therefore, experiments that directly test plant palatability and the traits underlying palatability along a temperature gradient are needed. Here we experimentally tested the impact of temperature on aquatic plant growth, plant chemical traits (including stoichiometry) and plant palatability. We cultured three aquatic plant species at three temperatures (15, 20, and 25 degrees C), measured growth parameters, determined chemical traits and performed feeding trial assays using the generalist consumer Lymnaea stagnalis (pond snail). We found that rising temperature significantly increased the growth of all three aquatic plants. Plant nitrogen (N) and phosphorus (P) content significantly decreased, and carbon (C):N and C:P stoichiometry increased as temperature increased, for both Potamogeton lucens and Vallisneria spiralis, but not for Elodea nuttallii. By performing the palatability test, we found that rising temperatures significantly decreased plant palatability in P lucens, which could be explained by changes in the underlying chemical plant traits. In contrast, the palatability of E nuttallii and V spiralis was not affected by temperature. Overall. P lucens and V spiralis were always more palatable than E. nuttallii. We conclude that warming generally stimulates aquatic plant growth, whereas the effects on chemical plant traits and plant palatability are species-specific. These results suggest that the outcome of the impact of temperature rise on macrophyte stoichiometry and palatability from single-species studies may not be broadly applicable. In contrast, the plant species tested consistently differed in palatability, regardless of temperature, suggesting that palatability may be more strongly linked to species identity than to intraspecific variation in plant stoichiometry.
  • Limnology

    Classifying nuisance submerged vegetation depending on ecosystem services

    Michiel Verhofstad, (Liesbeth) E.S. Bakker
    Throughout the world, mass development of native and non-native submerged macrophytes leads to nuisance problems for humans. However, often neither the type of nuisance nor the characteristics of nuisance vegetation have been uniformly quantified, leaving nuisance vegetation as a largely unsubstantiated qualification. The lack of a consensus about when submerged plants cause nuisance hampers comparative research on the environmental conditions leading to nuisance. Furthermore, defining and evaluating management goals to reduce nuisance caused by submerged plants are not possible when characteristics of the nuisance vegetation remain unquantified. In this study, we performed a literature review and gathered stakeholder information to identify (1) which problems are caused by nuisance submerged macrophytes, (2) which plant characteristics underlie `nuisance' and (3) and which species cause nuisance. We (4) synthesised this information into a framework to classify submerged vegetation as either `nuisance' or `non-nuisance' using a case study to illustrate the principles. We found that most nuisance problems that affect human use of the ecosystem can be grouped into problems for boat traffic, swimming, fishing and hydrological functioning of the system. Additionally, a multitude of ecological effects have also been reported, but these were outside of the scope of this study. Vegetation cover and canopy depth below the water surface are the main determinant characters for nuisance. Therefore, both invasive and native eutrophilic species with a vertical growth strategy are particularly problematic, but other species can also cause nuisance.
  • Journal of Applied Ecology

    Plant functional diversity and nutrient availability can improve restoration of floating fens via facilitation, complementarity and selection effects

    Jeroen P. van Zuidam, Casper van Leeuwen, (Liesbeth) E.S. Bakker, Jos T.A. Verhoeven, Stéphanie Ijff, Edwin T.H.M. Peeters, Bastiaan G. van Zuidam, Merel Soons
    Abstract Peat-forming wetlands, particularly floating fens that form the initial stages of these ecosystems, are declining globally due to excavation, dehydration and eutrophication. Restoration typically involves reestablishment of early-successional open-water stages, with oligotrophic conditions that are characteristic for these systems. However, restoration success is notoriously limited. A potential improvement may be to initiate succession by reintroducing of target plant species. Knowledge is therefore needed on (a) which plant functional groups should be re-introduced to stimulate fen formation; and (b) how to manage nutrient levels during restoration, considering that plant growth may be slow in oligotrophic conditions. We hypothesized that increasing functional diversity of introduced species would stimulate the formation of peat-forming target communities, their biomass accumulation and expansion onto open water. We also hypothesized that nutrient availability would mediate the relative contribution of specific functional groups to these effects. We investigated this in 36 artificial outdoor ponds by manipulating plant functional diversity (clonal dominants, clonal stress-tolerators and interstitials) on constructed rafts with fen-forming communities, and subjected these to a range of nutrient loadings over 2 years. Increasing functional diversity as well as increasing nutrient loadings had stimulating effects on plant biomass accumulation, cover formation and rhizome growth onto open water. Both complementarity (due to niche partitioning or facilitation) and selection effects were mechanisms underlying the diversity effect, with a constant relative importance over the entire range of nutrient availabilities. Different functional groups were important for biomass production at different nutrient availabilities. Rhizome formation by clonal stress-tolerators contributed disproportionately to open water colonization, identifying this functional group as key across all nutrient levels. Synthesis and applications. Restoration of floating fen communities can be stimulated during the first 2 years by introducing a high functional diversity of plant species. There include fast-growing clonal species, clonal stress-tolerators and interstitials, which facilitate each other. Restoration is dependent on the presence of clonal stress-tolerators such as Calla palustris, Comarum palustre and Menyanthes trifoliata for expansion onto the open water. Furthermore, restoration can start under a wide range of water nutrient levels, including eutrophic conditions.
  • Science of the Total Environment

    Success of lake restoration depends on spatial aspects of nutrient loading and hydrology

    Annette B.G. Janssen, Dianneke van Wijk, Luuk P.A. Van Gerven, (Liesbeth) E.S. Bakker, Bob Brederveld, Donald L. DeAngelis, Jan H. Janse, Wolf M. Mooij
    Many aquatic ecosystems have deteriorated due to human activities and their restoration is often troublesome. It is proposed here that the restoration success of deteriorated lakes critically depends on hitherto largely neglected spatial heterogeneity in nutrient loading and hydrology. A modelling approach is used to study this hypothesis by considering four lake types with contrasting nutrient loading (point versus diffuse) and hydrology (seepage versus drainage). By comparing the longterm effect of common restoration measures (nutrient load reduction, lake flushing or biomanipulation) in these four lake types, we found that restoration through reduction of nutrient loading is effective in all cases. In contrast, biomanipulation only works in seepage lakes with diffuse nutrient inputs, while lake flushing will even be counterproductive in lakes with nutrient point sources. The main conclusion of the presented analysis is that a priori assessment of spatial heterogeneity caused by nutrient loading and hydrology is essential for successful restoration of lake ecosystems.
  • Aquatic Botany

    Combined effects of shading and clipping on the invasive alien macrophyte Elodea nuttallii

    Liang He, (Liesbeth) E.S. Bakker, Marta M. Alirangues Nuñez, Sabine Hilt
    The response of macrophytes to herbivory and mowing in freshwater ecosystems is ambiguous. A recent study based on a plant growth model and a meta-analysis of field studies suggested that submerged macrophytes are more susceptible to plant removal by herbivory when additionally shaded by periphyton. Here, we test whether such synergistic effects of shading and herbivory or mowing can be experimentally confirmed. We used Elodea nuttallii, one of the alien invasive species of the highest concern in Europe. It is a preferred species by herbivorous water birds and is subject to mowing as a common management measure. We exposed E. nuttallii to four levels of clipping, with and without additional shading. Our results show a synergistic effect between shading and clipping for final shoot height of E. nuttallii and an additive effect for biomass, as enhanced branching compensated for shoot biomass losses by clipping in shaded treatments. Our results indicate that shading may help to maintain a lower canopy height of E. nuttallii when grazed by water birds or mown, but does not synergistically reduce total plant biomass. We conclude that the response of aquatic macrophytes to combined stress by shading and herbivory or mowing can differ among growth parameters and among species and is important to consider in aquatic plant management.
  • Ecology Letters

    More salt, please: global patterns, responses, and impact of foliar sodium in grasslands

    Elizabeth T. Borer, E. Lind, J Firn, Eric W. Seabloom, T Michael Anderson, (Liesbeth) E.S. Bakker, Lori A. Biederman, K.J. La Pierre, A.S. MacDougall, Joslin L. Moore, Anita C. Risch, Martin Schütz, Carly J. Stevens
    Sodium is unique among abundant elemental nutrients, because most plant species do not require it for growth or development, whereas animals physiologically require sodium. Foliar sodium influences consumption rates by animals and can structure herbivores across landscapes. We quantified foliar sodium in 201 locally abundant, herbaceous species representing 32 families and, at 26 sites on four continents, experimentally manipulated vertebrate herbivores and elemental nutrients to determine their effect on foliar sodium. Foliar sodium varied taxonomically and geographically, spanning five orders of magnitude. Site‐level foliar sodium increased most strongly with site aridity and soil sodium; nutrient addition weakened the relationship between aridity and mean foliar sodium. Within sites, high sodium plants declined in abundance with fertilisation, whereas low sodium plants increased. Herbivory provided an explanation: herbivores selectively reduced high nutrient, high sodium plants. Thus, interactions among climate, nutrients and the resulting nutritional value for herbivores determine foliar sodium biogeography in herbaceous‐dominated systems.
  • PLoS One

    Aquatic omnivores shift their trophic position towards increased plant consumption as plant stoichiometry becomes more similar to their body stoichiometry

    Peiyu Zhang, Reinier van den Berg, Casper van Leeuwen, Brigitte Blonk, (Liesbeth) E.S. Bakker
    Human induced eutrophication has strongly altered aquatic ecosystems. With increasing eutrophication, plant nutrient concentrations increase, making them more attractive as food for herbivores. However, most aquatic consumers are omnivorous. Ecological stoichiometry theory predicts that animals prefer to consume food which has a similar nutrient (N and P) composition or C:nutrient ratio compared to their own bodies, hence omnivorous animals may prefer to eat animal prey instead of plants. We asked whether aquatic omnivores would shift their diet towards more plant consumption when plants are more nutritious and their stoichiometry becomes more similar to the stoichiometry of the omnivore. We hypothesized that: (1) the omnivore increases plant consumption as the plant C:nutrient ratio decreases when there is only plant material available; (2) the omnivore generally prefers animal food over plant material; (3) the omnivore will increase its relative plant consumption as the plant C:nutrient ratio decreases, in the presence of animal food. As a model system, we used the pond snail Lymnaea stagnalis (omnivorous consumer), the aquatic plant Potamogeton lucens (plant food to the consumer, cultured at different nutrient regimes to obtain different plant C:nutrient ratios), and the crustacean Gammarus pulex (animal food to the consumer, using freshly dead individuals). When there was only plant material available, the consumers increased their relative consumption rate with decreasing plant C:nutrient ratio from no measurable amount to about 102 mg g-1 day-1. When plant material was offered simultaneously with animal food, even though the omnivores always preferred animal food over plant material, the omnivores still increased their relative intake of plant material as plant C:nutrient ratio decreased, from virtually nothing at the highest to on average 16% of their diet at the lowest plant C:nutrient ratio, with a maximum of 28%. Therefore, we conclude that as nutrient loading increases in aquatic ecosystems, plant-eating omnivorous animals may shift their trophic position towards increased plant consumption and alter the food web structure. As a result, we may observe increased top-down control on aquatic plants.
  • Hydrobiologia

    Plants in aquatic ecosystems: current trends and future directions

    Matthew T. O’Hare, Francisca C. Aguiar, Takashi Asaeda, (Liesbeth) E.S. Bakker, Patricia A. Chambers, John S. Clayton, Arnaud Elger, Teresa M. Ferreira, Elisabeth M. Gross, Iain D.M. Gunn, Angela M. Gurnell, Seppo Hellsten, Deborah E. Hofstra, Wei Li, Silvia Mohr, Sara Puijalon, Krzysztof Szoszkiewicz, Nigel J. Willby, Kevin A. Wood
    Aquatic plants fulfil a wide range of ecological roles, and make a substantial contribution to the structure, function and service provision of aquatic ecosystems. Given their well-documented importance in aquatic ecosystems, research into aquatic plants continues to blossom. The 14th International Symposium on Aquatic Plants, held in Edinburgh in September 2015, brought together 120 delegates from 28 countries and six continents. This special issue of Hydrobiologia includes a select number of papers on aspects of aquatic plants, covering a wide range of species, systems and issues. In this paper, we present an overview of current trends and future directions in aquatic plant research in the early twenty first century. Our understanding of aquatic plant biology, the range of scientific issues being addressed and the range of techniques available to researchers have all arguably never been greater; however, substantial challenges exist to the conservation and management of both aquatic plants and the ecosystems in which they are found. The range of countries and continents represented by conference delegates and authors of papers in the special issue illustrates the global relevance of aquatic plant research in the early twenty first century but also the many challenges that this burgeoning scientific discipline must address.
  • Global Change Biology

    Warming enhances sedimentation and decomposition of organic carbon in shallow macrophyte-dominated systems with zero net effect on carbon burial

    Mandy Velthuis, Sarian Kosten, Ralf C. Aben, Garabet Kazanjian, Sabine Hilt, Edwin T.H.M. Peeters, Ellen Van Donk, (Liesbeth) E.S. Bakker
    Temperatures have been rising throughout recent decades and are predicted to rise further in the coming century. Global warming affects carbon cycling in freshwater ecosystems, which both emit and bury substantial amounts of carbon on a global scale. Currently, most studies focus on the effect of warming on overall carbon emissions from freshwater ecosystems, while net effects on carbon budgets may strongly depend on burial in sediments. Here, we tested whether year‐round warming increases the production, sedimentation, or decomposition of particulate organic carbon and eventually alters the carbon burial in a typical shallow freshwater system. We performed an indoor experiment in eight mesocosms dominated by the common submerged aquatic plant Myriophyllum spicatum testing two temperature treatments: a temperate seasonal temperature control and a warmed (+4°C) treatment (n = 4). During a full experimental year, the carbon stock in plant biomass, dissolved organic carbon in the water column, sedimented organic matter, and decomposition of plant detritus were measured. Our results showed that year‐round warming nearly doubled the final carbon stock in plant biomass from 6.9 ± 1.1 g C in the control treatment to 12.8 ± 0.6 g C (mean ± SE), mainly due to a prolonged growing season in autumn. DOC concentrations did not differ between the treatments, but organic carbon sedimentation increased by 60% from 96 ± 9.6 to 152 ± 16 g C m−2 yaer−1 (mean ± SE) from control to warm treatments. Enhanced decomposition of plant detritus in the warm treatment, however, compensated for the increased sedimentation. As a result, net carbon burial was 40 ± 5.7 g C m−2 year−1 in both temperature treatments when fluxes were combined into a carbon budget model. These results indicate that warming can increase the turnover of organic carbon in shallow macrophyte‐dominated systems, while not necessarily affecting net carbon burial on a system scale.
  • Philosophical Transactions of the Royal Society B: Biological Sciences

    Trophic rewilding: impact on ecosystems under global change

    (Liesbeth) E.S. Bakker, Jens-Christian Svenning
    Human-induced global change is increasingly affecting life on our planet, including living conditions for humans themselves as well as the resources we depend on [1,2]. As a result, species diversity is strongly declining [3–5]. The Living Planet Index shows a 58% global decline in populations of amphibians, fish, reptiles, mammals and birds between 1970 and 2012, varying from 36 to 38% in terrestrial and marine ecosystems to 81% in freshwater habitat [6]. Habitat loss or degradation and overexploitation are the main causes of these steep declines. Since the worldwide expansion of modern humans (Homo sapiens) began, humans have overexploited vertebrates, with a bias to the largest animals being extirpated first, from the Late Pleistocene extinctions of terrestrial megafauna to the ongoing declines of terrestrial, marine and freshwater large-bodied animals [7–11]. There is increasing evidence that this global wildlife loss, or defaunation, does not only imply the loss of charismatic animals but also the functions they have in ecosystems [12–16]. To restore these missing functions, a novel ecological restoration technique has emerged, referred to as rewilding [17]. Rewilding aims to restore natural processes in ecosystems in general, and often focuses on re-introduction of missing large wildlife species or, in case these went extinct, their proxies [18]. Rewilding is increasingly implemented in practice globally, with a strong emphasis on Europe and the re-introduction of large herbivores [19,20].
  • Frontiers in Plant Science

    High grazing pressure of geese threatens conservation and restoration of reed belts

    (Liesbeth) E.S. Bakker, Ciska Veen, G. Ter Heerdt, Naomi Huig, Judith Sarneel
    Reed (Phragmites australis (Cav.) Trin. ex Steud.) beds are important habitat for marsh birds, but are declining throughout Europe. Increasing numbers of the native marsh bird, the Greylag goose (Anser anser L.), are hypothesized to cause reed bed decline and inhibit restoration of reed beds, but data are largely lacking. In this study, we experimentally tested the effect of grazing by Greylag geese on the growth and expansion of reed growing in belts along lake shorelines. After 5 years of protecting reed from grazing with exclosures, reed stems were over 4-fold denser and taller than in the grazed plots. Grazing pressure was intense with 50–100% of the stems being grazed among years in the control plots open to grazing. After 5 years of protection we opened half of the exclosures and the geese immediately grazed almost 100% of the reed stems. Whereas this did not affect the reed stem density, the stem height was strongly reduced and similar to permanently grazed reed. The next year geese were actively chased away by management from mid-March to mid-June, which changed the maximum amount of geese from over 2300 to less than 50. As a result, reed stem density and height increased and the reed belt had recovered over the full 6 m length of the experimental plots. Lastly, we introduced reed plants in an adjacent lake where no reed was growing and geese did visit this area. After two years, the density of the planted reed was six to nine-fold higher and significantly taller in exclosures compared to control plots where geese had access to the reed plants. We conclude that there is a conservation dilemma regarding how to preserve and restore reed belts in the presence of high densities of Greylag geese as conservation of both reed belts and high goose numbers seems infeasible. We suggest that there are three possible solutions for this dilemma: (1) effects of the geese can be mediated by goose population management, (2) the robustness of the reed marshes can be increased, and (3) at the landscape level, spatial planning can be used to configure landscapes with large reed bed reserves surrounded by unmown, unfertilized meadows.
  • Frontiers in Plant Science

    Response of Submerged Macrophyte Communities to External and Internal Restoration Measures in North Temperate Shallow Lakes

    Sabine Hilt, Marta M. Alirangues Nuñez, (Liesbeth) E.S. Bakker, Irmgard Blindow, Thomas A. Davidson, Mikael Gillefalk, Lars-Anders Hansson, Jan H. Janse, Annette B.G. Janssen, Erik Jeppesen, Timm Kabus, Andrea Kelly, Jan Köhler, Torben L. Lauridsen, Wolf M. Mooij, Ruurd Noordhuis, Geoff Phillips, Jacqueline Rücker, Hans-Heinrich Schuster, Martin Søndergaard, Sven Teurlincx, Klaus van de Weyer, Ellen Van Donk, Arno Waterstraat, Nigel J. Willby, Carl D. Sayer
    Submerged macrophytes play a key role in north temperate shallow lakes by stabilising clear-water conditions. Eutrophication has resulted in macrophyte loss and shifts to turbid conditions in many lakes. Considerable efforts have been devoted to shallow lake restoration in many countries, but long-term success depends on a stable recovery of submerged macrophytes. However, recovery patterns vary widely and remain to be fully understood. We hypothesize that reduced external nutrient loading leads to an intermediate recovery state with clear spring and turbid summer conditions similar to the pattern described for eutrophication. In contrast, lake internal restoration measures can result in transient clear-water conditions both in spring and summer and reversals to turbid conditions. Furthermore, we hypothesize that these contrasting restoration measures result in different macrophyte species composition, with added implications for seasonal dynamics due to differences in plant traits. To test these hypotheses, we analysed data on water quality and submerged macrophytes from 49 north temperate shallow lakes that were in a turbid state and subjected to restoration measures. To study the dynamics of macrophytes during nutrient load reduction, we adapted the ecosystem model PCLake. Our survey and model simulations revealed the existence of an intermediate recovery state upon reduced external nutrient loading, characterised by spring clear-water phases and turbid summers, whereas internal lake restoration measures often resulted in clear-water conditions in spring and summer with returns to turbid conditions after some years. External and internal lake restoration measures resulted in different macrophyte communities. The intermediate recovery state following reduced nutrient loading is characterised by a few macrophyte species (mainly pondweeds) that can resist wave action allowing survival in shallow areas, germinate early in spring, have energy-rich vegetative propagules facilitating rapid initial growth and that can complete their life cycle by early summer. Later in the growing season these plants are, according to our simulations, outcompeted by periphyton, leading to late-summer phytoplankton blooms. Internal lake restoration measures often coincide with a rapid but transient colonisation by hornworts, waterweeds or charophytes. Stable clear-water conditions and a diverse macrophyte flora only occurred decades after external nutrient load reduction or when measures were combined.
  • Hydrobiologia

    The effect of temperature on herbivory by the omnivorous ectotherm snail Lymnaea stagnalis

    Peiyu Zhang, Brigitte Blonk, Reinier van den Berg, (Liesbeth) E.S. Bakker
    Rising temperatures likely affect the trophic interactions in temperate regions as global warming progresses. An open question is how a temperature rise may affect consumer pressure and plant abundance in shallow aquatic ecosystems, where most consumers are omnivorous. Interestingly, herbivory (plant-eating) is more prevalent toward low latitudes in ectotherms such as fish and aquatic invertebrates, and this may be temperature driven. We used pond snails (Lymnaea stagnalis L.) as a model aquatic ectotherm species and tested their consumption of both animal prey (Gammarus pulex L.) and plant material (Potamogeton lucens L.) at three different temperatures (15, 20, and 25°C). Higher temperatures led to higher consumption rates by the omnivore on both plant food and animal prey when fed separately. When the food was offered simultaneously, the pond snails consistently preferred animal prey over plant material at all tested temperatures. However, the omnivore did consume plant material even though they had enough animal prey available to them. Based on our experiments, we conclude that with increasing temperatures, L. stagnalis will only increase their consumption rates but not change food preference. Further studies are needed to test the generality of our findings across aquatic species to predict the effect of warming on aquatic plant consumption.
  • Frontiers in Plant Science

    Mechanisms of invasion resistance of aquatic plant communities

    Antonella Petruzzella, J. Manschot, Casper van Leeuwen, Bart Grutters, (Liesbeth) E.S. Bakker
    Invasive plant species are among the major threats to freshwater biodiversity. Few experimental studies have investigated whether native plant diversity can provide biotic resistance to invaders in freshwater ecosystems. At small spatial scales, invasion resistance may increase with plant species richness due to a better use of available resources, leaving less available for a potential invader (Complementarity effect) and/or the greater probability to have a highly competitive (or productive) native species in the community (Selection effect). In submerged aquatic plant communities, we tested the following hypotheses: (1) invader establishment success is greatest in the absence of a native plant community; (2) lower in plant communities with greater native species richness, due to complementary and/or selection effects; and (3) invader establishment success would be lowest in rooted plant communities, based on the limiting similarity theory as the invader is a rooted submerged species. In a greenhouse experiment, we established mesocosms planted with 0 (bare sediment), 1, 2, and 4 submerged plant species native to NW Europe and subjected these to the South African invader Lagarosiphon major (Ridl.) Moss. We used two rooted (Myriophyllum spicatum L., Potamogeton perfoliatus L.) and two non-rooted native species (Ceratophyllum demersum L., Utricularia vulgaris L.) representing two distinct functional groups considering their nutrient acquisition strategy which follows from their growth form, with, respectively, the sediment and water column as their main nutrient source. We found that the presence of native vegetation overall decreased the establishment success of an alien aquatic plant species. The strength of this observed biotic resistance increased with increasing species richness of the native community. Mainly due to a selection effect, the native biomass of mixed communities overyielded, and this further lowered the establishment success of the invader in our experiment. The strongest biotic resistance was caused by the two native plant species that were of the same functional group, i.e., functionally most similar to the invader. These results support the prediction of Elton’s biotic resistance hypothesis in aquatic ecosystems and indicate that both species richness and functional group identity can play an important role in decreasing establishment success of alien plant species.
  • Nature Ecology and Evolution

    Change in dominance determines herbivore effects on plant biodiversity

    Sally E Koerner, Melinda D. Smith, Deron E Burkepile, Niall P Hanan, Meghan L Avolio, Scott L. Collins, Alan K Knapp, Nathan P Lemoine, Elisabeth J Forrestel, Stephanie Eby, Dave I Thompson, Gerardo A Aguado-Santacruz, John P Anderson, T Michael Anderson, Ayana Angassa, Sumanta Bagchi, (Liesbeth) E.S. Bakker, Gary Bastin, Lauren E Baur, Karen H Beard, Erik A Beever, Patrick J Bohlen, Elizabeth H Boughton, Don Canestro, Ariela Cesa, Enrique J. Chaneton, Jimin Cheng, Carla M D'Antonio, Claire Deleglise, Fadiala Dembélé, Josh Dorrough, David J Eldridge, Barbara Fernandez-Going, Silvia Fernández-Lugo, Lauchlan H. Fraser, Bill Freedman, Gonzalo García-Salgado, Jacob R Goheen, Liang-Dong Guo, Sean Husheer, Moussa Karembé, Johannes M. H. Knops, Tineke Kraaij, Andrew Kulmatiski, Minna-Maarit Kytöviita, Felipe Lezama, Gregory Loucougaray, Alejandro Loydi, Dan G Milchunas, Suzanne J Milton, John W Morgan, Claire Moxham, Kyle C Nehring, Han Olff, Todd M Palmer, Salvador Rebollo, Corinna Riginos, Anita C. Risch, Marta Rueda, Mahesh Sankaran, Takehiro Sasaki, Kathryn A Schoenecker, Nick L Schultz, Martin Schütz, Angelika Schwabe, Frances Siebert, Christian Smit, Karen A Stahlheber, Christian Storm, Dustin J Strong, Jishuai Su, Yadugiri V Tiruvaimozhi, Claudia Tyler, James Val, Martijn L. Vandegehuchte, Kari E Veblen, Lance T Vermeire, David Ward, Jianshuang Wu, Truman P Young, Qiang Yu, Tamara Jane Zelikova

    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.
  • Ecology

    Herbivore exclusion promotes a more stochastic plant community assembly in a natural grassland

    Juan Alberti, (Liesbeth) E.S. Bakker, R. van Klink, Han Olff, Christian Smit
    Both bottom-up (e.g. nutrients) and top-down (e.g. herbivory) forces structure plant communities, but it remains unclear how they affect the relative importance of stochastic and deterministic processes in plant community assembly. Moreover, different sized herbivores have been shown to have contrasting effects on community structure and function, but their effects on the processes governing community assembly (i.e. how they generate the impacts on structure) remain largely unknown. We evaluated the influence of bottom-up and top-down forces on the relative importance of deterministic and stochastic processes during plant community assembly. We used the data of a 7-year factorial experiment manipulating nutrient availability (ambient and increased) and the presence of vertebrate herbivores (> 1 kg) of different body size in a floodplain grassland in The Netherlands. We used a null model that describes a community composition expected by chance (i.e. stochastic assembly) and compared the plant community composition in the different treatments with this null model (the larger the difference, the more deterministically assembled). Our results showed that herbivore exclusion promoted a more stochastic plant community assembly, whereas increased nutrients played a relatively minor role in determining the relative importance of stochasticity in community assembly. Large herbivores facilitated intermediate-sized mammal herbivores, resulting in synergistic effects of enhanced grazing pressure and a more deterministic and convergent plant community assembly. We conclude that herbivores can act as strong deterministic forces during community assembly in natural systems. Our results also reveal that although large- and intermediate-sized mammal herbivores often have contrasting effects on many community and ecosystem properties, they can also synergistically homogenize plant communities.
  • Aquatic Invasions

    Potential for biotic resistance from herbivores to tropical and subtropical plant invasions in aquatic ecosystems

    Antonella Petruzzella, Bart Grutters, S.M. Tomaz, (Liesbeth) E.S. Bakker
    Invasions of tropical and subtropical aquatic plants threaten biodiversity and cause ecological and economic impacts worldwide.
    An urgent question is whether native herbivores are able to inhibit the spread of these alien species thus providing biotic resistance.
    The potential for biotic resistance to these plants depends on plant traits that affect palatability to herbivores, i.e., plant nutritional
    quality and the presence of secondary metabolites related to anti-herbivory defenses. Studies across latitudinal gradients suggest
    that aquatic plants from lower latitudes may be less nutritious and better defended than high latitude plants. Therefore, we
    hypothesized that native herbivores prefer temperate plants over plants from tropical and subtropical regions which would limit the
    strength of biotic resistance that native temperate herbivores can provide against alien tropical and subtropical plants. Drawing
    upon the published literature we (1) investigated whether native temperate herbivores reduce the establishment or performance of
    tropical and subtropical alien plants in the field, and (2) analyzed herbivore consumption of tropical and subtropical versus
    temperate plants in laboratory feeding trials. In our literature survey, we found only three field studies which, in contrast to our
    hypothesis, all demonstrated that the native herbivores (beavers, coots or generalist insect herbivores) significantly reduced the
    success of invading tropical and subtropical plant species. The analysis of the feeding trials yielded mixed results. Ten out of twelve
    feeding trials showed that (sub)tropical and temperate plants were consumed in equal amounts by both temperate and tropical
    generalist ectothermic herbivores. The remaining trials showed higher consumption rate of both temperate and tropical plants by
    tropical snails. Although a body of evidence suggests that tropical plants are nutritionally poor and better defended (i.e., less
    palatable) compared to temperate plants, we conclude that in the majority of cases, herbivores would eat tropical plants as much as
    temperate plants. Thus, in agreement with the available field studies, evidence suggests that there is potential for biotic resistance
    from native generalist herbivores to tropical invasive plants in non-tropical areas.
  • Freshwater Biology

    Periphyton density is similar on native and non-native plant species

    Bart Grutters, Elisabeth M. Gross, Ellen Van Donk, (Liesbeth) E.S. Bakker
    Non-native plants increasingly dominate the vegetation in aquatic ecosystems and thrive in eutrophic conditions. In eutrophic conditions, submerged plants risk being overgrown by epiphytic algae; however, if non-native plants are less susceptible to periphyton than natives, this would contribute to their dominance. Non-native plants may differ from natives in their susceptibility to periphyton growth due to differences in nutrient release, allelopathy and architecture. Yet, there is mixed evidence for whether plants interact with periphyton growth through nutrient release and allelopathy, or whether plants are neutral so that only their architecture matters for periphyton growth.
    We hypothesised that (1) non-native submerged vascular plants support lower periphyton density than native species, (2) native and non-native species are not neutral substrate for periphyton and interact with periphyton and (3) periphyton density increases with the plant structural complexity of plant species.
    We conducted an experiment in a controlled climate chamber where we grew 11 aquatic plant species and an artificial plant analogue in monocultures in buckets. These buckets were inoculated with periphyton that was collected locally from plants and hard substrate. Of the 11 living species, seven are native to Europe and four are non-native. The periphyton density on these plants was quantified after five weeks.
    We found that the periphyton density did not differ between non-native and native plants and was not related to plant complexity. Three living plant species supported lower periphyton densities than the artificial plant, one supported a higher periphyton density and the other plants supported similar densities. However, there was a strong negative correlation between plant growth and periphyton density.
    We conclude that the periphyton density varies greatly among plant species, even when these were grown under similar conditions, but there was no indication that the interaction with periphyton differs between native and non-native plant species. Hence, non-native plants do not seem to benefit from reduced periphyton colonisation compared to native species. Instead, certain native and non-native species tolerate eutrophic conditions well and as a consequence, they seem to host less periphyton than less tolerant species.
  • Functional Ecology

    Plant traits and plant biogeography control the biotic resistance provided by generalist herbivores

    Bart Grutters, Yvonne Roijendijk, W.C.E.P. Verberk, (Liesbeth) E.S. Bakker
    1.Globalization and climate change trigger species invasions and range shifts, which reshuffle communities at an exceptional rate and expose plant migrants to unfamiliar herbivores. Dominant hypotheses to predict plant success are based on evolutionary novelty: either herbivores are maladapted to consume novel plants (enemy release hypothesis), or novel plants are maladapted to deter herbivores (biotic resistance hypothesis). Since novelty can work both ways, it fails to consistently predict when herbivores will consume novel over non-novel plants. Surprisingly, the value of using plant traits to predict herbivore consumption of novel plants remains largely unexplored. We hypothesized that (1) plant traits explain generalist herbivore consumption rates of novel and non-novel plants, and (2) any effect of novelty will be grounded in consistent trait differences between native and novel plants. Lastly, we expected to find (3) differences in plant traits and plant consumption rates across latitude.

    2.To test these hypotheses, we measured the consumption rate of plant species for a tropical and a temperate generalist herbivore in controlled feeding trials by offering them a large variety of 40 plant species from different geographical origins. Therefore, whether a plant was novel depended on the herbivore used, allowing us to disentangle plant identity from plant novelty. We also measured plant chemical traits and determined whether traits, geographic origin or novelty best explained herbivore consumption rates.

    3.Both generalist herbivores consumed more of plants with a high nitrogen-to-phenolic compounds ratio, irrespective of the plant's novelty to the herbivore. A pattern of increasing plant's nitrogen-to-phenolics ratio with latitude could explain why both the tropical and temperate herbivore consumed more of plants from temperate regions. Plant novelty and its geographic origin no longer explained consumption rates once differences in nitrogen-to-phenolic compounds ratio were taken into account.

    4.We show that differences in plant traits along a latitudinal cline determine herbivore consumption rates, irrespective of whether plants are novel or familiar. Therefore, we propose that integrating evolutionary novelty theory with plant traits and biogeography will increase our understanding of the consequences of plant species migration beyond biogeographical barriers.
  • Aquatic Botany

    Mass development of monospecific submerged macrophyte vegetation after the restoration of shallow lakes: roles of light, sediment nutrient levels, and propagule density

    Michiel Verhofstad, Marta Maria Alirangues, Erik Reichman, Ellen Van Donk, Leon P. M. Lamers, (Liesbeth) E.S. Bakker
    Abstract After restoration, eutrophicated shallow freshwaters may show mass development of only one or two submerged macrophyte species, lowering biodiversity and hampering recreation. It is unclear which environmental factors govern this high percentage of the volume inhabited (PVI11 PVI: The percent of the water volume inhabited by submerged macrophytes. ) by submerged macrophytes, and whether the development of a more diverse, low canopy vegetation is likely to occur if dominant species decline in abundance. We hypothesized that (1) adequate light and high sediment nutrient availability leads to massive development of submerged macrophytes, and (2) that macrophyte species richness is low at high PVI, but that this is not caused by a lack of viable propagules of non-dominant species (especially charophytes). To test these hypotheses, fifteen shallow waters in the Netherlands were studied with respect to submerged vegetation (including propagules), water, and sediment characteristics. The probability of high submerged macrophyte PVI is highest in shallow waters where light availability in the water layer and phosphorus availability in the sediment are abundant. These conditions typically occur upon restoration of eutrophic waterbodies by reducing water nutrient loading or applying biomanipulation. Other factors, as top-down control, can additionally influence realised PVI. Viable propagules of species other than the dominant ones, including charophytes, were found in most of the sediments, indicating that once the dominant species declines, there is local potential for a diverse submerged vegetation to develop. Results can be used to predict when mass development occurs and to tackle the factors causing mass development.
  • Frontiers in Plant Science

    Impact of temperature and nutrients on carbon:nutrient tissue stoichiometry of submerged aquatic plants: an experiment and meta-analysis

    Mandy Velthuis, Emma van Deelen, Ellen Van Donk, Peiyu Zhang, (Liesbeth) E.S. Bakker
    Human activity is currently changing our environment rapidly, with predicted temperature increases of 1–5°C over the coming century and increased nitrogen and phosphorus inputs in aquatic ecosystems. In the shallow parts of these ecosystems, submerged aquatic plants enhance water clarity by resource competition with phytoplankton, provide habitat, and serve as a food source for other organisms. The carbon:nutrient stoichiometry of submerged aquatic plants can be affected by changes in both temperature and nutrient availability. We hypothesized that elevated temperature leads to higher carbon:nutrient ratios through enhanced nutrient-use efficiency, while nutrient addition leads to lower carbon:nutrient ratios by the luxurious uptake of nutrients. We addressed these hypotheses with an experimental and a meta-analytical approach. We performed a full-factorial microcosm experiment with the freshwater plant Elodea nuttallii grown at 10, 15, 20, and 25°C on sediment consisting of pond soil/sand mixtures with 100, 50, 25, and 12.5% pond soil. To address the effect of climatic warming and nutrient addition on the carbon:nutrient stoichiometry of submerged freshwater and marine plants we performed a meta-analysis on experimental studies that elevated temperature and/or added nutrients (nitrogen and phosphorus). In the microcosm experiment, C:N ratios of Elodea nuttallii decreased with increasing temperature, and this effect was most pronounced at intermediate nutrient availability. Furthermore, higher nutrient availability led to decreased aboveground C:P ratios. In the meta-analysis, nutrient addition led to a 25, 22, and 16% reduction in aboveground C:N and C:P ratios and belowground C:N ratios, accompanied with increased N content. No consistent effect of elevated temperature on plant stoichiometry could be observed, as very few studies were found on this topic and contrasting results were reported. We conclude that while nutrient addition consistently leads to decreased carbon:nutrient ratios, elevated temperature does not change submerged aquatic plant carbon:nutrient stoichiometry in a consistent manner. This effect is rather dependent on nutrient availability and may be species-specific. As changes in the carbon:nutrient stoichiometry of submerged aquatic plants can impact the transfer of energy to higher trophic levels, these results suggest that eutrophication may enhance plant consumption and decomposition, which could in turn have consequences for carbon sequestration.
  • Aquatic Botany

    Management and control methods of invasive alien freshwater aquatic plants: a review

    Andreas Hussner, I. Stiers, Michiel Verhofstad, (Liesbeth) E.S. Bakker, Bart Grutters, J. Haury, J.L.C.H. van Valkenburg, G. Brundu, J. Newman, John S. Clayton, L.W.J. Anderson, Deborah E. Hofstra
    Introduced invasive alien aquatic plants (IAAPs) threaten ecosystems due to their excessive growth and have both ecological and economic impacts. To minimize these impacts, effective management of IAAPs is required according to national or international laws and regulations (e.g. the new EU regulation 1143/2014). Prevention of the introduction of IAAPs is considered the most cost effective management option. If/when prevention fails, early detection and rapid response increases the likelihood of eradication of the IAAPs and can minimize on-going management costs. For effective weed control (eradication and/or reduction), a variety of management techniques may be used. The goal or outcome of management interventions may vary depending on the site (i.e. a single waterbody, or a region with multiple waterbodies) and the feasibility of achieving the goal with the tools or methods available. Broadly defined management goals fall into three different categories of, containment, reduction or nuisance control and eradication. Management of IAAP utilises a range of control methods, either alone or in combination, to achieve a successful outcome. Here we review the biological, chemical and mechanical control methods for IAAPs, with a focus on the temperate and subtropical regions of the world and provide a management diagram illustrating the relationships between the state of the ecosystem, the management goals, outcomes and tools.
  • Environmental Management

    Mowing Submerged Macrophytes in Shallow Lakes with Alternative Stable States: Battling the Good Guys?

    Jan J. Kuiper, Michiel Verhofstad, Evelien Louwers, (Liesbeth) E.S. Bakker, Bob Brederveld, Luuk P.A. Van Gerven, Annette B.G. Janssen, Jeroen J.M. de Klein, Wolf M. Mooij
    Submerged macrophytes play an important role in maintaining good water quality in shallow lakes. Yet extensive stands easily interfere with various services provided by these lakes, and harvesting is increasingly applied as a management measure. Because shallow lakes may possess alternative stable states over a wide range of environmental conditions, designing a successful mowing strategy is challenging, given the important role of macrophytes in stabilizing the clear water state. In this study, the integrated ecosystem model PCLake is used to explore the consequences of mowing, in terms of reducing nuisance and ecosystem stability, for a wide range of external nutrient loadings, mowing intensities and timings. Elodea is used as a model species. Additionally, we use PCLake to estimate how much phosphorus is removed with the harvested biomass, and evaluate the long-term effect of harvesting. Our model indicates that mowing can temporarily reduce nuisance caused by submerged plants in the first weeks after cutting, particularly when external nutrient loading is fairly low. The risk of instigating a regime shift can be tempered by mowing halfway the growing season when the resilience of the system is highest, as our model showed. Up to half of the phosphorus entering the system can potentially be removed along with the harvested biomass. As a result, prolonged mowing can prevent an oligo—to mesotrophic lake from becoming eutrophic to a certain extent, as our model shows that the critical nutrient loading, where the lake shifts to the turbid phytoplankton-dominated state, can be slightly increased.
  • Ecological Engineering

    Finding the harvesting frequency to maximize nutrient removal in a constructed wetland dominated by submerged aquatic plants

    Michiel Verhofstad, M.D.M. Poelen, M.M.L. Van Kempen, (Liesbeth) E.S. Bakker, Alfons J. P. Smolders
    Water quality is still poor in many freshwater ecosystems around the world as a result of anthropogenic nutrient loading. Constructed wetlands can be used to remove excess nutrients. In these wetlands, helophytes or free floating aquatic plants are traditionally used to absorb the nutrients. The nutrients are subsequently exported upon harvesting of the plants. However, rooted submerged plants may be more effective to extract nutrients from moderately eutrophicated ecosystems than helophytes or floating species.

    Here, we tested how the frequency of harvesting affected submerged biomass production, biomass nutrient content and the resulting amount of nutrients removed, as well as the vegetation composition and structure. Two Myriophyllum spicatum dominated shallow ponds, with moderately low surface water nutrient loading (∼5.6 mg N.m−2.d−1 and ∼1.32 mg P.m−2.d−1) were used. Each pond was subjected to four harvesting treatments: mowing 1x, 2x, 3 x or 5 x between May and September 2015.

    Harvesting 2 x or 3 x removed most biomass and nutrients, while mowing either 5 x or only once at the end of the growing season removed the lowest amount of nutrients from the system. Furthermore, the dominance of M. spicatum in the vegetation was best maintained in plots mown 2 x, while its cover declined in plots mown more frequently, resulting in an increase of charophyte abundance.

    We conclude that harvesting at an intermediate frequency is best when aiming to remove the maximum amount of nutrients under a moderately low nutrient loading. Harvesting more frequently may be a suitable management method to reduce dominance of M. spicatum in situations where it causes nuisance problems due to massive growth.
  • Aquatic Invasions

    Impact of native and non-native aquatic plants on methane emission and phytoplankton growth

    Bart Grutters, Ralf C. Aben, Sarian Kosten, (Liesbeth) E.S. Bakker
    Freshwater plants affect the ecosystem functioning of shallow aquatic ecosystems. However, because native plants are threatened
    by environmental change such as eutrophication, global warming and biological invasions, continued ecosystem functioning may
    be at risk. In this study, we explored how the growth of native and non-native plant species in eutrophic, warm conditions impacts
    two plant ecosystem functions: regulation of phytoplankton growth and methane emission. We expected that plants would inhibit
    phytoplankton growth, while for methane emission both inhibition and stimulation are possible. We conducted an outdoor
    experiment using monocultures of four native and four non-native freshwater plant species planted at three different densities, as
    well as a no-plant control. Monocultures of each species were planted in 65 L mesocosms and after three weeks of acclimatisation
    each mesocosm was inoculated with phytoplankton. Subsequently, we added nutrients twice a week for eight weeks, before
    harvesting the plant biomass. During these eight weeks, we measured chlorophyll-a concentration thirteen times and the diffusive
    methane emissions once after four weeks. The mesocosms amplified the temperature of a warm summer so that plants were
    exposed to higher-than-average temperatures. We found that five plant species lost biomass, two species increased their biomass
    only at the highest initial plant density (native Myriophyllum spicatum and non-native Lagarosiphon major) and a single species
    increased its biomass at all densities (on average 14 times its initial mass; amphibious non-native Myriophyllum aquaticum).
    Overall, the mean biomass change of non-natives was positive, whereas that of natives was negative. This difference in biomass
    change between native and non-native plants did not relate to overall differences in phytoplankton mass or diffusive methane
    emissions. In mesocosms where submerged plant species gained biomass, chlorophyll-a concentration was lower than in the noplant
    control and mesocosms with biomass loss. Diffusive methane emissions were highest in mesocosms where plants lost
    considerable biomass, likely because it increased substrate availability for methanogenesis. However, mesocosms where plant
    biomass increased had emissions similar to the no-plant control, hence we found no inhibitory effects of plant presence on
    diffusive methane emission. We conclude that plant growth in eutrophic, warm conditions varies strongly with plant identity. Our
    results furthermore suggest that plant identity determines whether the replacement of native by non-native freshwater plants will
    alter ecosystem functions such as regulation of phytoplankton growth and methane emission.
  • Frontiers of Earth Science

    The stoichiometry of nutrient release by terrestrial herbivores and its ecosystem consequences.

    Judith Sitters, (Liesbeth) E.S. Bakker, M. Veldhuis, Ciska Veen, Harry Olde Venterink, M.J. Vanni
    It is widely recognized that the release of nutrients by herbivores via their waste products strongly impacts nutrient availability for autotrophs. The ratios of nitrogen (N) and phosphorus (P) recycled through herbivore release (i.e., waste N:P) are mainly determined by the stoichiometric composition of the herbivore's food (food N:P) and its body nutrient content (body N:P). Waste N:P can in turn impact autotroph nutrient limitation and productivity. Herbivore-driven nutrient recycling based on stoichiometric principles is dominated by theoretical and experimental research in freshwater systems, in particular interactions between algae and invertebrate herbivores. In terrestrial ecosystems, the impact of herbivores on nutrient cycling and availability is often limited to studying carbon (C):N and C:P ratios, while the role of terrestrial herbivores in mediating N:P ratios is also likely to influence herbivore-driven nutrient recycling. In this review, we use rules and predictions on the stoichiometry of nutrient release originating from algal-based aquatic systems to identify the factors that determine the stoichiometry of nutrient release by herbivores. We then explore how these rules can be used to understand the stoichiometry of nutrient release by terrestrial herbivores, ranging from invertebrates to mammals, and its impact on plant nutrient limitation and productivity. Future studies should focus on measuring both N and P when investigating herbivore-driven nutrient recycling in terrestrial ecosystems, while also taking the form of waste product (urine or feces) and other pathways by which herbivores change nutrients into account, to be able to quantify the impact of waste stoichiometry on plant communities.
  • Aquatic Ecology

    Lake restoration by in-lake iron addition: A synopsis of iron impact on aquatic organisms and shallow lake ecosystems

    Internal phosphorus loading has become a major problem in many shallow freshwater lakes over the past decades due to the build-up of phosphorus stocks in the sediment. Iron is a natural capping agent which can enhance sediment P binding capacity, thus reducing P availability and shifting a lake from an algal to a macrophyte dominated state. Iron could, however, also impose toxic effects on the biota. We therefore provide a synopsis of iron toxicity studies and lake restoration measures using iron addition. Iron toxicity studies revealed that, even though iron is an essential nutrient for growth, when added in excess, it can negatively affect aquatic organisms. We found 13 studies testing the effect of iron addition as a restoration measure in the field (10) or using sediment from lakes and reservoirs in the laboratory (3). Twelve of the studies reported increased P retention after iron addition, which depended on the iron salts used and the concentrations added in two studies, whereas one study found no effect on P retention. Eight out of the nine field studies that reported biotic responses found reduced chlorophyll concentrations in the water column, whereas toxic effects of iron on organisms remained absent. Iron addition was most successful when external P loading, and concentrations of organic matter and sulphate were low as well as densities of sediment disturbing fish and crayfish. We conclude that iron addition can be a successful restoration method when these conditions are met.
  • Oikos

    Synergy between shading and herbivory triggers macrophyte loss and regime shifts in aquatic systems

    Bert Hidding, (Liesbeth) E.S. Bakker, Michiel J. M. Hootsmans, Sabine Hilt
    Macrophytes play a keystone role in shallow aquatic ecosystems. In lakes, macrophytes stabilize clear-water conditions with high biodiversity and their decline can cause a shift to a turbid state with lower biodiversity. Various mechanisms have been suggested as triggers of macrophyte collapse. Herbivory by waterfowl and fish seems to be one of the obvious factors, but the response of macrophytes to herbivory is ambiguous. We hypothesized that herbivory alone does not typically cause macrophyte collapse, but that shading from periphyton can enhance the effect of herbivores. Shading of macrophytes is supposed to increase with eutrophication due to changes in the top–down control cascading from fish via macroinvertebrates to periphyton. We elaborated on this idea by fitting a macrophyte growth model with different herbivore grazing and periphyton shading scenarios. In addition, we performed a meta-analysis on existing experimental herbivore exclosure studies with respect to periphyton growth. The model supported our proposed hypothesis and the reviewed field studies appeared to point in the same direction. We suggest that a significant herbivore impact may indicate a reduced resilience of vegetation to eutrophication, making it an early warning signal for an imminent macrophyte collapse leading to a sudden shift of the system to turbid conditions.
  • Aquatic Ecology

    Impact of water level fluctuations on cyanobacterial blooms: Options for management

    (Liesbeth) E.S. Bakker, Sabine Hilt
    Climate change can promote harmful cyanobacteria blooms in eutrophic waters through increased droughts or flooding. In this paper, we explore how water-level fluctuations affect the occurrence of cyanobacterial blooms, and based on the observations from case studies, we discuss the options and pitfalls to use water-level fluctuations for lake and reservoir management. A drawdown in summer causes an increase in retention time and increased water column nutrient concentrations and temperature of shallow water layers, which may lead to severe cyanobacterial blooms. This effect can potentially be counteracted by the positive response of submerged macrophytes, which compete for nutrients with cyanobacteria, with a higher chance of cyanobacterial blooms under eutrophic conditions. The balance between dominance by submerged macrophytes or cyanobacteria is temperature sensitive with stronger positive effects of drawdown as inhibition of cyanobacterial blooms expected in colder climates. Complete drying out reduces the amount of cyanobacteria in the water column after refilling, with lower water nutrient concentrations, lower fish biomass, lower abundance of cyanobacteria, higher transparency, and higher cover of submerged plants compared to lakes and reservoirs that did not dry out. Water-level rise as response to flooding has contrasting effects on the abundance of cyanobacteria depending on water quality. We conclude that water-level fluctuation management has potential to mitigate cyanobacterial blooms. However, the success will depend strongly on ecosystem properties, including morphometry, sediment type, water retention time, quality of inlet water, presence of submerged vegetation or propagules, abundance of fish, and climate.
  • Ecography

    Assessing the role of large herbivores in the structuring and functioning of freshwater and marine angiosperm ecosystems

    (Liesbeth) E.S. Bakker, Jordi F. Pagès, Rohan Arthur, Teresa Alcoverro
    While large herbivores can have strong impacts on terrestrial ecosystems, much less is known of their role in aquatic systems. We reviewed the literature to determine: (1) which large herbivores (>10 kg) have a (semi-)aquatic lifestyle and are important consumers of submerged vascular plants, (2) their impact on submerged plant abundance and species composition and (3) their ecosystem functions.We grouped herbivores according to diet, habitat selection and movement ecology: (1) Fully aquatic species, either resident or migratory (manatees, dugongs, turtles), (2) Semi-aquatic species that live both in water and on land, either resident or migratory (swans), (3) Resident semi-aquatic species that live in water and forage mainly on land (hippopotamuses, beavers, capybara), (4) Resident terrestrial species with relatively large home ranges that frequent aquatic habitats (cervids, water buffalo, lowland tapir).Fully aquatic species and swans have the strongest impact on submerged plant abundance and species composition. They may maintain grazing lawns. Because they sometimes target belowground parts, their activity can result in local collapse of plant beds. Semi-aquatic species and turtles serve as important aquatic-terrestrial linkages, by transporting nutrients across ecosystem boundaries. Hippopotamuses and beavers are important geomorphological engineers, capable of altering the land and hydrology at landscape scales. Migratory species and terrestrial species with large home ranges are potentially important dispersal vectors of plant propagules and nutrients. Clearly, large aquatic herbivores have strong impacts on associated species and can be critical ecosystem engineers of aquatic systems, with the ability to modify direct and indirect functional pathways in ecosystems. While global populations of large aquatic herbivores are declining, some show remarkable local recoveries with dramatic consequences for the systems they inhabit. A better understanding of these functional roles will help set priorities for the effective management of large aquatic herbivores along with the plant habitats they rely on.This article is protected by copyright. All rights reserved.
  • Proceedings of the National Academy of Sciences of the United States of America

    Global nutrient transport in a world of giants

    C.E. Doughty, J. Roman, S. Faurby, A. Wolf, A. Haque, (Liesbeth) E.S. Bakker, Yadvinder Malhi, J. Dunning, J.C. Svenning
    The past was a world of giants, with abundant whales in the sea and large animals roaming the land. However, that world came to an end following massive late-Quaternary megafauna extinctions on land and widespread population reductions in great whale populations over the past few centuries. These losses are likely to have had important consequences for broad-scale nutrient cycling, because recent literature suggests that large animals disproportionately drive nutrient movement. We estimate that the capacity of animals to move nutrients away from concentration patches has decreased to about 8% of the preextinction value on land and about 5% of historic values in oceans. For phosphorus (P), a key nutrient, upward movement in the ocean by marine mammals is about 23% of its former capacity (previously about 340 million kg of P per year). Movements by seabirds and anadromous fish provide important transfer of nutrients from the sea to land, totalling ∼150 million kg of P per year globally in the past, a transfer that has declined to less than 4% of this value as a result of the decimation of seabird colonies and anadromous fish populations. We propose that in the past, marine mammals, seabirds, anadromous fish, and terrestrial animals likely formed an interlinked system recycling nutrients from the ocean depths to the continental interiors, with marine mammals moving nutrients from the deep sea to surface waters, seabirds and anadromous fish moving nutrients from the ocean to land, and large animals moving nutrients away from hotspots into the continental interior.
  • Functional Ecology

    Locomotion during digestion changes current estimates of seed dispersal kernels by fish

    Casper van Leeuwen, Rosanne Beukeboom, Bart A. Nolet, (Liesbeth) E.S. Bakker, B.J.A. Pollux
    Dispersal of seeds by animals is an important mechanism regulating plant diversity, range expansions and invasions. Many birds, mammals, fish, and reptiles regularly ingest, transport and excrete viable seeds (known as endozoochory). The effectiveness of endozoochory is modelled in dispersal kernels: functions that describe seed shadows in the landscape by combining movement of animals with experimentally obtained seed retention times and survival. Currently, dispersal kernels use experimental data from resting animals, yet only moving animals disperse seeds. Although physical activity is known to affect digestive processes, little is known on how and to what extent this may influence current estimates of endozoochory. Activity may either prolong seed retention in the animal's gut (locomotion-priority mode hypothesis) or may not affect seed excretion rate (digestion-priority mode hypothesis), and may affect seed survival and germination positively or negatively. We tested how activity alters dispersal estimates in fish. We compared the seed dispersal potential of two riparian plant species (Carex acuta and C. riparia) by the common carp (Cyprinus carpio) subjected to three different activity levels: low (basal metabolic rate, BMR), medium (2×BMR), or high activity (3×BMR). Physical activity of the fish did not affect the number of intact retrieved seeds over 15 h of activity, but significantly affected seed retrieval patterns over time for both seed species. More active fish started seed excretion about 1 h later and kept excreting seeds at least 2 h longer. Effects of gut passage on germination could only be tested for C. acuta, where it reduced the percentage of germinating seeds by 22%, independent of the activity level. Seeds ingested by the fish germinated on average 3.5 days later than non-ingested control seeds. Seed retention times did not affect the timing of germination. Our results support the locomotion-priority mode hypothesis, and show that modelling dispersal kernels using parameters from inactive fish may underestimate potential dispersal distances. Because a trade-off between physical activity and digestive physiology is likely common in animals, it should be taken into account in future modelling of endozoochorous seed dispersal kernels. This article is protected by copyright. All rights reserved.
  • Hydrobiologia

    The impact of bird herbivory on macrophytes and the resilience of the clear-water state in shallow lakes: a model study

    Shallow lakes have the potential to switch between two alternative stable states: a clear macrophyte-dominated and a turbid phytoplankton-dominated state. Observational and experimental studies show that in some lakes herbivory by birds may severely decrease macrophyte biomass, while in other lakes, the removed biomass by herbivory is compensated by regrowth. These contradictory outcomes might arise because of interplay between top-down control by bird herbivory and bottom-up effects by nutrient loading on macrophytes. Here, we use the ecosystem model PCLake to study top-down and bottom-up control of macrophytes by coots and nutrient loading. Our model predicted that (1) herbivory by birds lowers the critical nutrient loading at which the regime shift occurs; (2) bird impact on macrophyte biomass through herbivory increases with nutrient loading; and (3) improved food quality enhances the impact of birds on macrophytes, thus decreasing the resilience of the clear-water state even further. The fact that bird herbivory can have a large impact on macrophyte biomass and can facilitate a regime shift implies that the presence of waterfowl should be taken into account in the estimation of critical nutrient loadings to be used in water quality management.
  • Hydrobiologia

    Insect herbivory on native and exotic aquatic plants: phosphorus and nitrogen drive insect growth and nutrient release

    Bart Grutters, E.M. Gross, (Liesbeth) E.S. Bakker
    Eutrophication and globalisation facilitate the dominance of exotic plants in aquatic ecosystems worldwide. Aquatic omnivores can provide biotic resistance to plant invasions, but little is known about whether obligate aquatic herbivores can do the same. Herbivores such as insects can decimate aquatic vegetation, but may not be able to consume exotic plants due to their more or less specialised nature of feeding. We experimentally tested the larval feeding of an aquatic insect, the moth Parapoynx stratiotata, on eleven submerged plant species, from either native or exotic origin. We also tested whether insect herbivory stimulates nutrient and organic matter release, thus affecting water quality. Larvae of P. stratiotata consumed seven out of eleven plant species, and their growth was related to plant nutrient content and stoichiometry. However, larvae had no preference for either native or exotic macrophytes, and their plant preference was not related to the measured plant traits, but was possibly driven by secondary metabolites. Through plant consumption, caterpillars induced brownification and phosphate release, and the intensity thereof varied among plant species, but not between native and exotic plants. In conclusion, P. stratiotata showed strong feeding preferences demonstrating that aquatic insects can directly and indirectly alter water quality and vegetation composition.
  • Aquatic Botany

    Herbivory on freshwater and marine macrophytes: a review and perspective

    (Liesbeth) E.S. Bakker, Kevin A. Wood, Jordi F. Pagès, Ciska Veen, Marjolijn J.A. Christianen, Luis Santamaría, Bart A. Nolet, Sabine Hilt
    Until the 1990s, herbivory on aquatic vascular plants was considered to be of minor importance, and the predominant view was that freshwater and marine macrophytes did not take part in the food web: their primary fate was the detritivorous pathway. In the last 25 years, a substantial body of evidence has developed that shows that herbivory is an important factor in the ecology of vascular macrophytes across freshwater and marine habitats. Herbivores remove on average 40-48% of plant biomass in freshwater and marine ecosystems, which is typically 5-10 times greater than reported for terrestrial ecosystems. This may be explained by the lower C:N stoichiometry found in submerged plants. Herbivores affect plant abundance and species composition by grazing and bioturbation and therewith alter the functioning of aquatic ecosystems, including biogeochemical cycling, carbon stocks and primary production, transport of nutrients and propagules across ecosystem boundaries, habitat for other organisms and the level of shoreline protection by macrophyte beds. With ongoing global environmental change, herbivore impacts are predicted to increase. There are pressing needs to improve our management of undesirable herbivore impacts on macrophytes (e.g. leading to an ecosystem collapse), and the conflicts between people associated with the impacts of charismatic mega-herbivores. While simultaneously, the long-term future of maintaining both viable herbivore populations and plant beds should be addressed, as both belong in complete ecosystems and have co-evolved in these long before the increasing influence of man. Better integration of the freshwater, marine, and terrestrial herbivory literatures would greatly benefit future research efforts.
  • Aquatic Botany

    Effects of warming on Potamogeton crispus growth and tissue stoichiometry in the growing season

    Peiyu Zhang, (Liesbeth) E.S. Bakker, M. Zhang, J. Xu
    Increased water temperature due to climate change may affect macrophyte phenology and nutrient content. In experimentally heated mesocosms the emergence and growth of Potamogeton crispus shoots under ambient and increased temperatures (+4.5 °C) were tracked over 55 days. At the end of the experiment we measured the C, N and P content of the P. crispus leaves. The results indicate that warming advanced the emergence of P. crispus shoots by approximately 10 days, whereas the final number of shoots and plant biomass were similar in ambient and heated tanks. Furthermore, warming influenced the ecological stoichiometry of this plant significantly. Leaf C and N content were both less in the heated tanks resulting in an increase in C:N ratios, whereas P content and C:P and N:P ratios were not affected.
  • Proceedings of the National Academy of Sciences of the United States of America

    Combining paleo-data and modern exclosure experiments to assess the impact of megafauna extinctions on woody vegetation

    (Liesbeth) E.S. Bakker, J.L. Gill, C.N. Johnson, F.W.M. Vera, C.J. Sandom, Gregory P. Asner, J.C. Svenning
    Until recently in Earth history, very large herbivores (mammoths, ground sloths, diprotodons, and many others) occurred in most of the World’s terrestrial ecosystems, but the majority have gone extinct as part of the late-Quaternary extinctions. How has this large-scale removal of large herbivores affected landscape structure and ecosystem functioning? In this review, we combine paleo-data with information from modern exclosure experiments to assess the impact of large herbivores (and their disappearance) on woody species, landscape structure, and ecosystem functions. In modern landscapes characterized by intense herbivory, woody plants can persist by defending themselves or by association with defended species, can persist by growing in places that are physically inaccessible to herbivores, or can persist where high predator activity limits foraging by herbivores. At the landscape scale, different herbivore densities and assemblages may result in dynamic gradients in woody cover. The late-Quaternary extinctions were natural experiments in large-herbivore removal; the paleoecological record shows evidence of widespread changes in community composition and ecosystem structure and function, consistent with modern exclosure experiments. We propose a conceptual framework that describes the impact of large herbivores on woody plant abundance mediated by herbivore diversity and density, predicting that herbivore suppression of woody plants is strongest where herbivore diversity is high. We conclude that the decline of large herbivores induces major alterations in landscape structure and ecosystem functions.
  • Landschap

    Effecten en beheer van uitheemse waterplanten in Nederlandse wateren

    Bart Grutters, (Liesbeth) E.S. Bakker, W.C.E.P. Verberk
    Uitheemse soorten bedreigen de biodiversiteit en de levering van ecosysteemdiensten. Daarom worden miljarden euro’s uitgegeven om deze soorten te bestrijden. Maar soms kunnen uitheemse planten belangrijk zijn als voedsel, beschutting of habitat voor inheemse soorten. Een vergelijking van functies van inheemse en uitheemse planten ontbreekt echter. Voor waterplanten hebben wij een dergelijke vergelijking gemaakt om tot een gedegen beheerstrategie te komen.
  • PLoS One

    Native and non-native plants provide similar refuge to invertebrate prey, but less than artificial plants

    Bart Grutters, B.J.A. Pollux, W.C.E.P. Verberk, (Liesbeth) E.S. Bakker
    Non-native species introductions are widespread and can affect ecosystem functioning by altering the structure of food webs. Invading plants often modify habitat structure, which may affect the suitability of vegetation as refuge and could thus impact predator-prey dynamics. Yet little is known about how the replacement of native by non-native vegetation affects predator-prey dynamics. We hypothesize that plant refuge provisioning depends on (1) the plant’s native status, (2) plant structural complexity and morphology, (3) predator identity, and (4) prey identity, as well as that (5) structurally similar living and artificial plants provide similar refuge. We used aquatic communities as a model system and compared the refuge provided by plants to macroinvertebrates (Daphnia pulex, Gammarus pulex and damselfly larvae) in three short-term laboratory predation experiments. Plant refuge provisioning differed between plant species, but was generally similar for native (Myriophyllum spicatum, Ceratophyllum demersum, Potamogeton perfoliatus) and non-native plants (Vallisneria spiralis, Myriophyllum heterophyllum, Cabomba caroliniana). However, plant refuge provisioning to macroinvertebrate prey depended primarily on predator (mirror carp: Cyprinus carpio carpio and dragonfly larvae: Anax imperator) and prey identity, while the effects of plant structural complexity were only minor. Contrary to living plants, artificial plant analogues did improve prey survival, particularly with increasing structural complexity and shoot density. As such, plant rigidity, which was high for artificial plants and one of the living plant species evaluated in this study (Ceratophyllum demersum), may interact with structural complexity to play a key role in refuge provisioning to specific prey (Gammarus pulex). Our results demonstrate that replacement of native by structurally similar non-native vegetation is unlikely to greatly affect predator-prey dynamics. We propose that modification of predator-prey interactions through plant invasions only occurs when invading plants radically differ in growth form, density and rigidity compared to native plants.
  • Ecological Engineering

    Fighting internal phosphorus loading: An evaluation of the large scale application of gradual Fe-addition to a shallow peat lake

    Anne Immers, (Liesbeth) E.S. Bakker, Ellen Van Donk, G. Ter Heerdt, Jeroen Geurts, Steven A.J. Declerck
    Abatement of external phosphorus (P) loading and biomanipulation are measures that are often applied with the aim to restore a macrophyte dominated clearwater state in turbid, anthropogenically eutrophied lakes. The recovery of such lakes, however, is often hampered by ‘internal eutrophication’, as a result of the release of historically accumulated P from the sediment into the water column. One way to combat this internal P loading is by adding iron (Fe) into the lake, which naturally binds to phosphate. Although studied in the laboratory or mesocosms, the effects of iron addition on a whole-lake scale are largely
    unknown. In this study we therefore compiled lake monitoring data to evaluate the effect of a gradual dose of 33 g Fe m2 on the water quality and biotic communities (phytoplankton, zooplankton and macrophytes) of Lake Terra Nova. During and after the Fe-addition, we also carried out assays to evaluate the effect of the Fe-addition on sediment P-release rates. Lake Terra Nova is a eutrophied, shallow peaty lake that has been subjected to biomanipulation measures for 10 years.
    The large scale addition of iron during 2010 and 2011 resulted in a substantial reduction of dissolved P, suspended matter (SM), phytoplankton biomass and relative Cyanobacterial biomass, whereas macrophytes reappeared. Fe-addition also resulted in strongly reduced sediment P-mobilisation rates.
    Nevertheless, reductions of water column TP in response to the Fe-addition were short-lived. This discrepancy between the observed TP-levels in the water column and sediment P-release rates could indicate that sustained loading with external P and interactions of chemical compounds with Fe may jeopardize long term restoration success by depleting the water column reservoir of reactive Fe. Ecological processes can in addition enhance this process by shunting P from the sediment to the water column.
  • Aquatic Botany

    Flooding tolerance and horizontal expansion of wetland plants: facilitation by floating mats?

    Bert Hidding, Judith Sarneel, (Liesbeth) E.S. Bakker
    Water level fluctuations (WLF) can be important disturbances promoting the diversity of riparian plant communities, but are currently absent from many managed aquatic ecosystems. A lack of WLF is thought to reduce plant diversity and hamper hydrosere succession. However, a positive impact of WLF on plant diversity may crucially depend on nutrient availability and the presence of a potential ecosystem engineer, the floating plant Stratiotes aloides, that may provide structural support to riparian plants. We tested the interactive effects of 40 cm flooding, presence of S. aloides and sediment nutrient availability (N and P) on growth and horizontal expansion of eight wetland plant species in a 10 week experiment. Seven out of eight species showed a significant elongation response to flooding. Compared to stagnant water levels, flooding in combination with high nutrient availability decreased horizontal expansion in two short species and increased it in two tall species, whereas flooding decreased horizontal expansion in two other short species under both nutrient levels. In this 10 week experiment, we observed no effect of S. aloides on the measured plant parameters. This experiment shows short-term negative effects of flooding on most of the short species. On the long-term, we hypothesize that improvements in water quality and seedling recruitment due to drawdown may result in net positive effects of WLF in the riparian zone, but as the species that were rare in the field happened to be short, care should be taken to maintain rare species when allowing more WLF.
  • Ecosystems

    Herbivores enforce sharp boundaries between terrestrial and aquatic ecosystems

    Judith Sarneel, Naomi Huig, Ciska Veen, W. Rip, (Liesbeth) E.S. Bakker
    The transitions between ecosystems (ecotones) are often biodiversity hotspots, but we know little about the forces that shape them. Today, often sharp boundaries with low diversity are found between terrestrial and aquatic ecosystems. This has been attributed to environmental factors that hamper succession. However, ecosystem properties are often controlled by both bottom-up and top-down forces, but their relative importance in shaping riparian boundaries is not known. We hypothesize that (1) herbivores may enforce sharp transitions between terrestrial and aquatic ecosystems by inhibiting emergent vegetation expansion and reducing the width of the transition zone and (2) the vegetation expansion, diversity, and species turnover are related to abiotic factors in the absence of herbivores, but not in their presence. We tested these hypotheses in 50 paired grazed and ungrazed plots spread over ten wetlands, during two years. Excluding grazers increased vegetation expansion, cover, biomass, and species richness. In ungrazed plots, vegetation cover was negatively related to water depth, whereas plant species richness was negatively related to the vegetation N:P ratio. The presence of (mainly aquatic) herbivores overruled the effect of water depth on vegetation cover increase but did not interact with vegetation N:P ratio. Increased local extinction in the presence of herbivores explained the negative effect of herbivores on species richness, as local colonization rates were unaffected by grazing. We conclude that (aquatic) herbivores can strongly inhibit expansion of the riparian vegetation and reduce vegetation diversity over a range of environmental conditions. Consequently, herbivores enforce sharp boundaries between terrestrial and aquatic ecosystems.
  • Journal of Ecology

    Hydrology, shore morphology and species traits affect seed dispersal, germination and community assembly in shoreline plant communities

    Casper van Leeuwen, Judith Sarneel, José van Paassen, W.J. Rip, (Liesbeth) E.S. Bakker
    Summary 1.Seed dispersal and germination are two primary processes influencing plant community assembly. On freshwater shores, water levels regulate both processes. However, it is still unclear how water levels, shore morphology and species traits interactively affect seed dispersal and germination, and how these interactions determine plant community assembly. We hypothesize that a drawdown water regime enhances seed establishment compared to a year-round stable water level, that this increases species richness and diversity, and that this is modulated by species traits and shore morphology. 2.Germination of 20 wetland plant species with different dispersal capacities (floating capacity expressed as seed floatation half-time) and soil moisture preferences for germination (Ellenberg F) was tested on artificial shores in 24 outdoor ponds in two complementary experiments over 8 weeks. The ‘dispersal experiment’ tested the effect of water regime on recruitment of hydrochorously dispersing seeds. The ‘seed bank experiment’ tested the effect of water regime on germination from a sown seed bank, on steep and gradual shores. 3.In the dispersal experiment, the drawdown regime increased recruitment and species richness. Longer floating species colonized a larger shoreline section. Soil moisture preference for germination did not determine colonization patterns. 4.In the seed bank experiment, the drawdown regime increased the number of seedlings on gradual sloping shores, but not on steep shores. The number of germinating seedlings corresponded to the area subjected to the drawdown regime in both shore types. Species richness was not affected by water regime or shore morphology, and species traits did not determine shoreline colonization. Most seeds germinated in moist soil conditions for all species. 5.Synthesis. A spring drawdown instead of stable water regime stimulates establishment of hydrochorously dispersing seeds in temperate wetlands, leading to higher species richness and diversity. Germination from the seed bank is more affected by water regime and shore surface than by the tested species traits. Species traits, water levels and shore morphology together determine wetland plant community assembly, with dispersal as the main driver of seedling community diversity. Water-level regulations and shore morphology can be used to influence plant communities in wetland restoration.
  • Oikos

    Grazing-induced changes in plant–soil feedback alter plant biomass allocation

    Large vertebrate herbivores, as well as plant–soil feedback interactions are important drivers of plant performance, plant community composition and vegetation dynamics in terrestrial ecosystems. However, it is poorly understood whether and how large vertebrate herbivores and plant–soil feedback effects interact. Here, we study the response of grassland plant species to grazing-induced legacy effects in the soil and we explore whether these plant responses can help us to understand long-term vegetation dynamics in the field. In a greenhouse experiment we tested the response of four grassland plant species, Agrostis capillaris, Festuca rubra, Holcus lanatus and Rumex acetosa, to field-conditioned soils from grazed and ungrazed grassland. We relate these responses to long-term vegetation data from a grassland exclosure experiment in the field. In the greenhouse experiment, we found that total biomass production and biomass allocation to roots was higher in soils from grazed than from ungrazed plots. There were only few relationships between plant production in the greenhouse and the abundance of conspecifics in the field. Spatiotemporal patterns in plant community composition were more stable in grazed than ungrazed grassland plots, but were not related to plant–soil feedbacks effects and biomass allocation patterns. We conclude that grazing-induced soil legacy effects mainly influenced plant biomass allocation patterns, but could not explain altered vegetation dynamics in grazed grasslands. Consequently, the direct effects of grazing on plant community composition (e.g. through modifying light competition or differences in grazing tolerance) appear to overrule indirect effects through changes in plant–soil feedback
  • Aquatic Botany

    Iron addition as a measure to restore water quality: Implications for macrophyte growth

    Anne Immers, K. Vendrig, Bas Ibelings, Ellen Van Donk, G. Ter Heerdt, Jeroen Geurts, (Liesbeth) E.S. Bakker
    Eutrophication of shallow lakes in North-West Europe has resulted in cyanobacterial blooms, turbid water, and a decline in submerged macrophytes. Even though external inputs of phosphorus (P) are declining, internal loading of P from the sediment may delay the recovery of these aquatic ecosystems. Iron can be a useful chemical binding agent to combat internal P loading in shallow lakes, but may potentially be harmful for macrophyte growth. We tested whether iron addition as a restoration measure harms the growth of submerged macrophytes. We hypothesized that this depends on the iron dosage and the rooting strategy of the macrophytes. We experimentally tested the effects of Fe (FeCl3) on the submerged macrophytes Potamogeton pectinatus L. and Elodea nuttallii (Planch.) H. St. John. Iron was dosed at a concentration of 20 g Fe m−2 and 40 g Fe m−2 to the surface water or to both the surface water and sediment. E. nuttallii growth was not affected by iron addition, whereas P. pectinatus growth significantly decreased with increasing iron concentrations. Nonetheless, biomass of both species increased in all treatments relative to starting conditions. During the experiment, propagules sprouted from a propagule bank in the sediment including species with a high conservation value and this spontaneous emergence was not influenced by increasing iron concentrations. We conclude that adding iron(III)chloride in dosages of 20–40 g m−2 may reduce growth of some macrophyte species, but does not prevent overall macrophyte recovery. It may however affect macrophyte community composition due to differential responses of macrophyte species to iron addition.
  • Oecologia

    Experimental evidence for enhanced top-down control of freshwater macrophytes with nutrient enrichment

    The abundance of primary producers is controlled by bottom-up and top-down forces. Despite the fact that there is consensus that the abundance of freshwater macrophytes is strongly influenced by the availability of resources for plant growth, the importance of top-down control by vertebrate consumers is debated, because field studies yield contrasting results. We hypothesized that these bottom-up and top-down forces may interact, and that consumer impact on macrophyte abundance depends on the nutrient status of the water body. To test this hypothesis, experimental ponds with submerged vegetation containing a mixture of species were subjected to a fertilization treatment and we introduced consumers (mallard ducks, for 8 days) on half of the ponds in a full factorial design. Over the whole 66-day experiment fertilized ponds became dominated by Elodea nuttallii and ponds without extra nutrients by Chara globularis. Nutrient addition significantly increased plant N and P concentrations. There was a strong interactive effect of duck presence and pond nutrient status: macrophyte biomass was reduced (by 50 %) after the presence of the ducks on fertilized ponds, but not in the unfertilized ponds. We conclude that nutrient availability interacts with top-down control of submerged vegetation. This may be explained by higher plant palatability at higher nutrient levels, either by a higher plant nutrient concentration or by a shift towards dominance of more palatable plant species, resulting in higher consumer pressure. Including nutrient availability may offer a framework to explain part of the contrasting field observations of consumer control of macrophyte abundance.
  • Journal of Applied Ecology

    Windows of opportunity for germination of riparian species after restoring water level fluctuations: a field experiment with controlled seed banks

    Judith Sarneel, R.H. Janssen, W.J. Rip, I. Bender, (Liesbeth) E.S. Bakker
    Restoration activities aiming at increasing vegetation diversity often try to stimulate both dispersal and germination. In wetlands, dispersal and germination are coupled as water and water level fluctuations (WLF) simultaneously influence seed transport and germination conditions (soil moisture). Water regime shifts have been shown to affect vegetation composition. However, the interactions between WLF, dispersal and subsequent germination as drivers of such changes are still poorly understood, especially within the complexity of a field situation. We tested the effect of soil moisture on ten riparian species in the greenhouse and sowed these species on 135 field locations in nine wetlands with recently restored WLF. We used quantile regressions to test the effects of WLF on the window of opportunity for germination from sown seeds and other seeds naturally dispersed to our plots, as well as on community diversity. Soil moisture significantly affected germination both in the greenhouse and in the field. In the complexity of a field situation, a flooding depth just below the soil level, an intermediate flooding duration and a high flooding frequency provided the best opportunities for maximal germination. This was because these conditions enhanced germination from the seed bank as well as increasing germination from dispersed seeds. Seedling diversity showed identical patterns. Other known (i.e., light conditions) and unknown factors played a role as we found low and variable germination, even under optimal conditions. We found evidence that WLF can affect vegetation zonation as flooded seedling communities contained more species with high moisture affinity. Synthesis and applications. Water level fluctuations provide clear windows of opportunity for germination both from the seed bank and from dispersed seeds. Water regime changes are therefore likely to strongly affect recruitment opportunities and subsequent community assembly in riparian ecosystems, for instance through climate change or management. Water level fluctuations can be used as management tool to stimulate plant recruitment and seedling diversity in riparian wetlands.
  • Ecology

    Testing the Stress Gradient Hypothesis in herbivore communities: facilitation peaks at intermediate nutrient levels

    (Liesbeth) E.S. Bakker, I. Dobrescu, D. Straile, M. Holmgren
    The role of positive interactions in structuring plant and animal communities is increasingly recognized but the generality of current theoretical models has remained practically unexplored in animal communities. The Stress Gradient Hypothesis predicts a linear increase in the intensity of facilitation as environmental conditions become increasingly stressful, whereas other theoretical models predict a maximum at intermediate environmental stress. We tested how competition and facilitation between herbivores change over a manipulated gradient of nutrient availability. We studied the effect of grazing by pond snails (Lymnaea stagnalis L.) as bulk grazers on aquatic caterpillars (Acentria ephemerella Denis & Schiffermüller) as small specialist grazers along an experimental gradient of environmental nutrient concentration. Higher nutrient levels increased overall total plant biomass but induced a shift towards dominance of filamentous algae at the expense of macrophytes. Facilitation of caterpillars by snail presence peaked at intermediate nutrient levels. Both caterpillar biomass and caterpillar grazing on macrophytes were highest at intermediate nutrient levels. Snails facilitated caterpillars possibly by removing filamentous algae and increasing access to the macrophyte resource, whereas they did not affect macrophyte biomass or C:nutrient ratios, a measure of food quality. We conclude that competition and facilitation in herbivore communities change along nutrient availability gradients that affect plant biomass and community composition. Understanding how interspecific interactions may change in strength and direction along environmental gradients is important to predict how the diversity and structure of communities may respond to the introduction or removal of herbivore species in ecosystems. Read More:
  • Hydrobiologia

    Restoring macrophyte diversity in shallow temperate lakes: biotic versus abiotic constraints

    (Liesbeth) E.S. Bakker, Judith Sarneel, Ramesh Gulati, Z. Liu, Ellen Van Donk
    Although many lake restoration projects have led to decreased nutrient loads and increased water transparency, the establishment or expansion of macrophytes does not immediately follow the improved abiotic conditions and it is often unclear whether vegetation with high macrophyte diversity will return. We provide an overview of the potential bottlenecks for restoration of submerged macrophyte vegetation with a high biodiversity and focus on the biotic factors, including the availability of propagules, herbivory, plant competition and the role of remnant populations. We found that the potential for restoration in many lakes is large when clear water conditions are met, even though the macrophyte community composition of the early 1900s, the start of humaninduced large-scale eutrophication in Northwestern Europe, could not be restored. However, emerging charophytes and species rich vegetation are often lost due to competition with eutrophic species. Disturbances such as herbivory can limit dominance by eutrophic species and improve macrophyte diversity. We conclude that it is imperative to study the role of propagule availability more closely as well as the biotic interactions including herbivory and plant competition. After abiotic conditions are met, these will further determine macrophyte diversity and define what exactly can be restored and what not.
  • Perspectives in Plant Ecology, Evolution and Systematics

    An integrated perspective to explain nitrogen mineralization in grazed ecosystems

    Maarten Schrama, Ciska Veen, (Liesbeth) E.S. Bakker, J.L. Ruifrok, Jan P. Bakker, H. Olff
    Large herbivores are key drivers of nutrient cycling in ecosystems worldwide, and hence they have an important influence on the productivity and species composition in plant communities. Classical theories describe that large herbivores can accelerate or decelerate nitrogen (N) mineralization by altering the quality and quantity of resource input (e.g. dung, urine, plant litter) into the soil food web. However, in many situations the impact of herbivores on N mineralization cannot be explained by changes in resource quality and quantity. In this paper, we aim to reconcile observations of herbivores on N mineralization that were previously regarded as contradictory. We conceptually integrate alternative pathways via which herbivores can alter N mineralization. We illustrate our new integrated perspective by using herbivore-induced soil compaction and subsequent changes in soil moisture and soil aeration as an example. We show that the net effect of herbivores on mineralization depends on the balance between herbivore-induced changes in soil physical properties and changes in the quality and quantity of resource input into the soil food web. For example, soil compaction by herbivores can limit oxygen or water availability in wet and dry soils respectively, particularly those with a fine texture. This can result in a reduction in N mineralization regardless of changes in resource quality or quantity. In such systems the plant community will shift towards species that are adapted to waterlogging (anoxia) or drought, respectively. In contrast, soils with intermediate moisture levels are less sensitive to compaction. In these soils, N mineralization rates are primarily associated with changes in resource quality and quantity. We conclude that our integrated perspective will help us to better understand when herbivores accelerate or decelerate soil nutrient cycling and improve our understanding of the functioning of grazed ecosystems
  • Journal of Insect Behavior

    A device to study the behavioral responses of zooplankton to food quality and quantity

    Tibor Bukovinszky, Nico Helmsing, R.A. Grau, (Liesbeth) E.S. Bakker, T. Martijn Bezemer, Matthijs Vos, H. Uittenhout, Anthony M. Verschoor
    In order to explore the behavioral mechanisms underlying aggregation of foragers on local resource patches, it is necessary to manipulate the location, quality and quantity of food patches. This requires careful control over the conditions in the foraging arena, which may be a challenging task in the case of aquatic resourceconsumer systems, like that of freshwater zooplankton feeding on suspended algal cells. We present an experimental tool designed to aid behavioral ecologists in exploring the consequences of resource characteristics for zooplankton aggregation behavior and movement decisions under conditions where the boundaries and characteristics (quantity and quality) of food patches can be standardized. The aggregation behavior of Daphnia magna and D. galeata x hyalina was tested in relation to i) the presence or absence of food or ii) food quality, where algae of high or low nutrient (phosphorus) content were offered in distinct patches. Individuals of both Daphnia species chose tubes containing food patches and D. galeata x hyalina also showed a preference towards food patches of high nutrient content. We discuss how the described equipment complements other behavioral approaches providing a useful tool to understand animal foraging decisions in environments with heterogeneous resource distributions.
  • PLoS One

    Invasive crayfish threaten the development of submerged macrophytes in lake restoration

    J.E.M. Van der Wal, M. Dorenbosch, Anne Immers, C. Vidal Forteza, Jeroen Geurts, Edwin T.H.M. Peeters, B. Koese, (Liesbeth) E.S. Bakker
    Submerged macrophytes enhance water transparency and aquatic biodiversity in shallow water ecosystems. Therefore, the return of submerged macrophytes is the target of many lake restoration projects. However, at present, north-western European aquatic ecosystems are increasingly invaded by omnivorous exotic crayfish. We hypothesize that invasive crayfish pose a novel constraint on the regeneration of submerged macrophytes in restored lakes and may jeopardize restoration efforts. We experimentally investigated whether the invasive crayfish (Procambarus clarkii Girard) affects submerged macrophyte development in a Dutch peat lake where these crayfish are expanding rapidly. Seemingly favourable abiotic conditions for macrophyte growth existed in two 0.5 ha lake enclosures, which provided shelter and reduced turbidity, and in one lake enclosure iron was added to reduce internal nutrient loading, but macrophytes did not emerge. We transplanted three submerged macrophyte species in a full factorial exclosure experiment, where we separated the effect of crayfish from large vertebrates using different mesh sizes combined with a caging treatment stocked with crayfish only. The three transplanted macrophytes grew rapidly when protected from grazing in both lake enclosures, demonstrating that abiotic conditions for growth were suitable. Crayfish strongly reduced biomass and survival of all three macrophyte species while waterfowl and fish had no additive effects. Gut contents showed that crayfish were mostly carnivorous, but also consumed macrophytes. We show that P. clarkii strongly inhibit macrophyte development once favourable abiotic conditions for macrophyte growth are restored. Therefore, expansion of invasive crayfish poses a novel threat to the restoration of shallow water bodies in north-western Europe. Prevention of introduction and spread of crayfish is urgent, as management of invasive crayfish populations is very difficult.
  • Freshwater Biology

    Aquatic grazers reduce the establishment and growth of riparian plants along an environmental gradient

    Ciska Veen, Judith Sarneel, Lone Ravensbergen, Naomi Huig, José van Paassen, W. Rip, (Liesbeth) E.S. Bakker
    Summary The establishment of riparian plants is determined by abiotic conditions and grazing, although it is usually presumed that the former are most important. We tested the impact of aquatic grazers on the survival and growth of establishing riparian plants and whether the impact of grazing interacts with abiotic conditions. We conducted an experiment across 10 Dutch wetlands, covering a large range of water depth and nutrient availability. We introduced 1-year-old plants of an emergent (common reed, Phragmites australis) and a floating (water soldier, Stratiotes aloides) species in individual enclosures (n = 5 per site) that excluded predominantly waterbirds, which were the most abundant grazers, and on adjacent unprotected plots. Survival and growth were measured during one growing season. Grazing reduced growth (as biomass) of Phragmites and Stratiotes by a mean of 25 and 60%, respectively. Grazing decreased survival of Stratiotes, but not of Phragmites. Shallow water, water-level fluctuations, eutrophic conditions and enough light favoured both growth and survival of Phragmites. Growth of Stratiotes was unaffected by these factors, but they reduced its survival. For both species, grazing effects on biomass were consistent across environmental conditions, but for Phragmites, grazing effects on survival were influenced by abiotic conditions. We conclude that aquatic grazers significantly reduce the establishment and growth of macrophytes in the riparian zone over a wide range of environmental conditions.
  • Hydrobiologia

    Iron addition as a shallow lake restoration measure: impacts on charophyte growth

    Anne Immers, M.T. Van der Sande, R.M. Van der Zande, Jeroen Geurts, Ellen Van Donk, (Liesbeth) E.S. Bakker
    Eutrophication has caused a decline of charophyte species in many shallow lakes in Europe. Even though external inputs of phosphorus are declining, internal loading of P from the sediment seems to delay the recovery of these systems. Iron is a useful chemical binding agent to combat internal phosphorus loading. However, the effects of iron addition on charophytes are not yet known. In this study we experimentally tested the potential toxicity of iron(III)chloride (FeCl3) on two different charophytes, Chara virgata Kützing and Chara globularis Thuiller added at the concentration of 20 g Fe m−2 and 40 g Fe m−2 to the surface water. C. virgata growth was not significantly affected, whereas C. globularis growth significantly decreased with increasing iron concentrations. Nonetheless, biomass of both species increased in all treatments relative to starting conditions. The decrease of C. globularis biomass with high iron additions may have been caused by a drop in pH and alkalinity in combination with iron induced light limitation. Iron addition over a longer time scale, however, will not cause this rapid drop in pH. Therefore, we conclude that adding iron(III)chloride in these amounts to the surface water of a lake can potentially be a useful restoration method.
  • Freshwater Biology

    Effects of contrasting omnivorous fish on submerged macrophyte biomass in temperate lakes: a mesocosm experiment

    M. Dorenbosch, (Liesbeth) E.S. Bakker
    1.Freshwater fish can affect aquatic vegetation directly by consuming macrophytes or indirectly by changing water quality. However, most fish in the temperate climate zone have an omnivorous diet. The impact of fish as aquatic herbivores in temperate climates therefore remains unclear and depends on their dietary flexibility. 2.We tested the effects of a flexible omnivore and an herbivore on aquatic vegetation by comparing the effects of rudd (Scardinius erythrophthalmus, the most herbivorous fish in temperate climates) with grass carp (Ctenopharyngodon idella) in a mesocosm pond study. Exclosures distinguished herbivorous effects of fish on submerged macrophytes from indirect effects through changes in water quality, whereas stable isotope food-web analysis provided information on fish diets. 3.We hypothesised that rudd, with its flexible diet and preference for animal food items, would only indirectly affect macrophytes, whereas grass carp, with its inflexible herbivorous diet, would directly affect macrophyte biomass. 4.Only grass carp significantly reduced macrophyte biomass through consumption. Rudd had no effect. Food-web analysis indicated that rudd predominantly consumed animal prey, whereas grass carp included more plants in their diet, although they also consumed animal prey. Grass carp significantly affected water quality, resulting in lowered pH and increased N-NH4 concentrations, whereas more periphyton growth was observed in the presence of rudd. However, the indirect non-herbivorous effects of both fish species had no effect on macrophyte biomass. 5.Both fish species should be considered as omnivores. Despite the fact that rudd is the most herbivorous fish in the western European climate zone, its effect on submerged macrophyte biomass is not substantial at natural densities and current temperatures.
  • Basic and Applied Ecology

    Host location success of root-feeding nematodes in patches that differ in size and quality: A belowground release-recapture experiment

    Tibor Bukovinszky, (Liesbeth) E.S. Bakker, Ciska Raaijmakers, Anthony M. Verschoor, T. Martijn Bezemer
    Resource patchsize and patch nutritional quality are both important factors influencing local densities of herbivores. The responses of herbivores to resource patchsize have been mostly studied in aboveground plant–insect interactions, whereas belowground organisms have received little attention. We studied responses of different root-feedingnematode species associated with marram grass (Ammophila arenaria (L.) Link) to resource patchsize and quality. Different nematode species were released in experimental mesocosms filled with dune sand in which we established marram grass patches of varying sizes. Half of the patches of small, medium and large size were fertilized to test if immigration probabilities of nematodes depended on patch quality. We tested the hypotheses that (1) nematodes should aggregate on larger patches and (2) colonization of patches would also depend on patch nutritional quality, with higher nematoderecapture rates expected in fertilized patches. Two species (Helicotylenchus pseudorobustus, Hemicycliophora thornei) of the five released species were recaptured in the experiment. The fraction of nematodes immigrating into the rhizosphere of a plant patch increased with patchsize (i.e. root biomass), which was in line with predictions of the Resource Concentration Hypothesis. When fractions were recalculated to represent recapture rates per liter of soil, recapture rates of nematodes did not differ among patchsizes, indicating that the increase in recapture rates was directly proportional to the increase in patchsize. This suggests that the process through which nematodes located patches was not distinguishable from a random process where entering patches is based on random encounters with patch boundaries. In contrast to our expectation, fertilization had a strong negative effect on patch responses of both nematode species. Our study represents an approach that may be used to explore whether belowground biota behave in similar ways as aboveground biota, in order to determine how perceived differences in environments affect ecological interactions.
  • PLoS One

    The Good, the Bad and the Plenty: Interactive Effects of Food Quality and Quantity on the Growth of Different Daphnia Species

    Tibor Bukovinszky, Anthony M. Verschoor, Nico Helmsing, T. Martijn Bezemer, (Liesbeth) E.S. Bakker, Matthijs Vos, Lisette de Senerpont Domis
    Effects of food quality and quantity on consumers are neither independent nor interchangeable. Although consumer growth and reproduction show strong variation in relation to both food quality and quantity, the effects of food quality or food quantity have usually been studied in isolation. In two experiments, we studied the growth and reproduction in three filter-feeding freshwater zooplankton species, i.e. Daphnia galeata x hyalina, D. pulicaria and D. magna, on their algal food (Scenedesmus obliquus), varying in carbon to phosphorus (C:P) ratios and quantities (concentrations). In the first experiment, we found a strong positive effect of the phosphorus content of food on growth of Daphnia, both in their early and late juvenile development. Variation in the relationship between the P-content of animals and their growth rate reflected interspecific differences in nutrient requirements. Although growth rates typically decreased as development neared maturation, this did not affect these species-specific couplings between growth rate and Daphnia P-content. In the second experiment, we examined the effects of food quality on Daphnia growth at different levels of food quantity. With the same decrease in P-content of food, species with higher estimated P-content at zero growth showed a larger increase in threshold food concentrations (i.e. food concentration sufficient to meet metabolic requirements but not growth). These results suggest that physiological processes such as maintenance and growth may in combination explain effects of food quality and quantity on consumers. Our study shows that differences in response to variation in food quality and quantity exist between species. As a consequence, species-specific effects of food quality on consumer growth will also determine how species deal with varying food levels, which has implications for resource-consumer interactions.
  • Basic and Applied Ecology

    Effects of nutrient additions and macrophyte composition on invertebrate community assembly and diversity in experimental ponds.

    Steven A.J. Declerck, (Liesbeth) E.S. Bakker, Bart van Lith, A.P. Kersbergen, Ellen Van Donk
    Macrophytes and nutrient loading are two factors that can strongly determine the diversity and composition of aquatic invertebrate communities. Both factors may also interact, because macrophyte species may be differentially affected by nutrients. Macrophyte community characteristics, such as species composition, morphotype and biomass have the potential to mediate the response of invertebrate communities to nutrient loading. In 36 newly constructed experimental ponds,weorthogonally combined three macrophyte community types (Chara-, Potamogeton- and Elodea-dominated) with two levels of nutrient additions (no addition and an addition of 0.5 mg P and 3mg N/L per week) and studied community assembly in three functional groups of invertebrates (epiphytic macroinvertebrates, littoral and pelagic crustacean zooplankton). Macrophyte biomass was negatively affected by nutrient addition. General linear models indicated negative responses of species richness in the zooplankton functional groups to nutrient addition and phytoplankton chlorophyll-a, but demonstrated no effects of macrophyte community type. Conversely, macroinvertebrate taxon richness differed among macrophyte community types but showed no response to nutrient enrichment. Macrophyte biomass correlated positively with the richness of littoral zooplankton and macroinvertebrates and was a better predictor of these diversity variables than macrophyte community type. Overall, our results indicate that lake management practices that aim at obtaining a nutrient poor and macrophyte dominated clear water state contribute also to the maintenance of aquatic invertebrate diversity.
  • Ecology

    Aquatic herbivores facilitate the emission of methane from wetlands

    Wetlands are significant sources of atmospheric methane. Methane produced by microbes enters roots and escapes to the atmosphere through the shoots of emergent wetland plants. Herbivorous birds graze on helophytes, but their effect on methane emission remains unknown. We hypothesized that grazing on shoots of wetland plants can modulate methane emission from wetlands. Diffusive methane emission was monitored inside and outside bird exclosures, using static flux chambers placed over whole vegetation and over single shoots. Both methods showed significantly higher methane release from grazed vegetation. Surface-based diffusive methane emission from grazed plots was up to five times higher compared to exclosures. The absence of an effect on methane-cycling microbial processes indicated that this modulating effect acts on the gas transport by the plants. Modulation of methane emission by animal–plant–microbe interactions deserves further attention considering the increasing bird populations and changes in wetland vegetation as a consequence of changing land use and climate change.
  • Freshwater Biology

    Herbivory in omnivorous fishes: effect of presence of plant secondary metabolites and prey stoichiometry

    M. Dorenbosch, (Liesbeth) E.S. Bakker
    1. Many animals that consume freshwater macrophytes are omnivorous (i.e., they include both plant and animal matter in their diet). For invertebrate omnivorous consumers, selection of macrophyte species depends partly on the presence of secondary metabolites in plants, plant carbon/nutrient balances and/or physical structure of plants. However, little is known about the mechanisms influencing consumption of macrophytes in aquatic vertebrates. 2. For two fish species, the omnivorous rudd (Scardinius erythrophthalmus) and herbivorous grass carp (Ctenopharyngodon idella), feeding preferences were determined in three choice experiments. We tested (i) whether the presence of secondary metabolites and macrophyte stoichiometry affects macrophyte species selection by fish, (ii) the importance of macrophyte stoichiometry by manipulating the macrophytes experimentally and (iii) the rate of herbivory when the most palatable macrophyte is offered simultaneously with a common animal prey. 3. In a choice experiment with five species of submerged macrophytes (Callitriche sp., Chara globularis, Elodea nuttallii, Myriophyllum spicatum and Potamogeton pectinatus), Myriophyllum was clearly consumed least by both fishes, which strongly correlated with the highest phenolic concentration of this macrophyte. Additionally, a significant negative relationship was found between consumption and C : N ratio of the five macrophytes. The two most consumed macrophytes also had the lowest dry matter concentration (DMC). 4. In a second choice experiment, the C : N ratio of the least (Myriophyllum) and most (Potamogeton) palatable plants was manipulated by growing the macrophytes under fertilised and unfertilised conditions and subsequently feeding them to rudd. The avoidance of consumption of the chemically defended Myriophyllum by rudd was partly alleviated by the lowered C : N ratio. 5. The third choice experiment showed that both fishes preferred animal prey (the amphipod Gammarus pulex) over the most palatable macrophyte (Potamogeton) when offered simultaneously. The C : N ratio of the amphipods was about half that of the lowest C : N ratio measured in the macrophytes. Consumption by the fishes could not clearly be related to C : P or N : P ratios of prey items in any of the experiments. 6. We conclude that omnivorous fish avoid macrophytes that are chemically defended. However, when these defences are only minor, stoichiometry (C : N ratio) in combination with DMC may be a determining factor for consumption by vertebrate facultative herbivores.
  • Basic and Applied Ecology

    Effect of macrophyte community composition and nutrient enrichment on plant biomass and algal blooms.

    Submerged freshwater macrophytes decline with increasing eutrophication. This has consequences for ecosystem processes in shallow lakes and ponds as macrophytes can reduce algal blooms under eutrophic conditions. We hypothesize that the productivity of submerged vegetation, biomass change under eutrophication and the suppression of algal blooms may be affected by macrophyte community composition. To test our hypothesis, we established three macrophyte community types in 36 fishless experimental ponds: one dominated by the oligotrophic species Chara globularis, one dominated by the eutrophic species Potamogeton pectinatus and a diverse vegetation which became co-dominated by Elodea nuttallii and C. globularis, and we fertilized half of the ponds. The macrophyte communities produced different amounts of biomass and they responded differently to fertilization. The community dominated by Potamogeton produced the lowest overall biomass, but was not affected by nutrient addition. The communities dominated by Chara and co-dominated by Elodea and Chara produced more than four-fold the amount of biomass produced in Potamogeton communities under oligotrophic conditions, but were strongly negatively affected by nutrient addition. Phytoplankton abundance did not differ significantly among the plant community types, but showed large variation within community types. There was a significant negative relationship between spring macrophyte biomass and the probability of summer algal blooms. The occurrence of algal blooms coincided with low daphnid densities and high pH (>10). We conclude that the macrophyte community composition, characterized by the dominant species, strongly affected the amount of biomass production as well as the short-term response of the vegetation to nutrient enrichment. Macrophyte community composition had no direct effect on algal blooms, but can affect the occurrence of algal blooms indirectly as these occurred only in ponds with low (
  • Aquatic Botany

    Differences in tolerance of pondweeds and charophytes to vertebrate herbivores in a shallow Baltic estuary

    Bert Hidding, (Liesbeth) E.S. Bakker, F. Keuper, Thijs de Boer, Peter De Vries, Bart A. Nolet
    It has been suggested that herbivorous waterfowl may be important in shaping aquatic plant communities in shallow wetlands. As such, a shift from canopy forming pondweeds to bottom-dwelling charophytes in a formerly turbid pondweed dominated lake has been partly attributed to waterfowl herbivory. Here we study the separate and combined effects of both belowground herbivory in spring by whooper swans and Bewick ‘s swans, and grazing in summer by waterfowl and fish on the community composition in a shallow Baltic estuary during one year. The macrophyte community was dominated by charophytes (mainly Chara aspera) with Potamogeton pectinatus and Najas marina present as subdominants. Other species were rare. Both spring and summer herbivory had no effect on total plant biomass. However, P. pectinatus was more abundant in plots that were closed to spring and summer herbivores. N. marina was more abundant in grazed plots, whereas Chara spp. biomass remained unaffected. Probably belowground propagules of both C. aspera and P. pectinatus were consumed by swans but since C. aspera bulbils were numerous it may have compensated for the losses. P. pectinatus may not have fully recovered from foraging on tubers and aboveground biomass. Our results are in line with other studies in Chara dominated lakes, which found no effect of grazing on summer aboveground Chara biomass, whereas several studies report strong effects of herbivory in lakes dominated by P. pectinatus.
  • Basic and Applied Ecology

    Effects of cattle and rabbit grazing on clonal expansion of spiny shrubs in wood-pastures

    C. Smit, (Liesbeth) E.S. Bakker, M.E.F. Apol, H. Olff
    Spiny shrubs protect non-defended plants against herbivores. Therefore, they play a role for the diversity in grazed ecosystems. While the importance of these keystone nurse shrubs is presently recognized, little is known about the factors controlling them. This knowledge is required to understand the functioning of grazed ecosystems and for sustainable management. We studied effects of cattle and rabbits on clonal expansion of Prunus spinosa in two ancient wood-pastures in the Netherlands. At each site we set up five blocks in grassland perpendicular to the edges of mature Prunus thickets, each block containing three herbivore treatments: (1) open-to-cattle-and-rabbits, (2) open to rabbits, cattle excluded, (3) cattle and rabbits excluded. We monitored the number and volume of Prunus ramets from 1998 to 2000 and again in 2003, 3 years after exclosure-removal to restore grazing. For 1998–2000 ramet volume, but not ramet number, differed between treatments. Ramet volume was highest when both cattle and rabbits were excluded. Ramet volume did not differ between grazing by rabbits or cattle and rabbits combined, indicating that rabbits alone may be as effective in inhibiting clonal expansion as cattle and rabbits combined. Three years after exclosure-removal ramet number and volume had increased in all treatments. Number of ramets remained unaffected by (former) treatments. Ramet volume remained highest in the former cattle-plus-rabbits exclusion treatment, differing significantly from the ‘open-to-cattle-and-rabbits’ treatment. So, once successfully established during herbivore absence, further expansion is not prevented by cattle and rabbit grazing. This study shows that vertebrate herbivory controls the keystone nurse-shrub in wood-pastures: combined cattle and rabbit grazing, and notably rabbits alone, inhibit expansion. Temporary herbivore absence allows expansion of ramets, which persists after herbivore-reappearance. Sustainable management of wood-pastures should allow spatial-temporal fluctuations of herbivore densities, leading to increased vegetation structure and associated biodiversity.
  • Oikos

    Cross-site comparison of herbivore impact on nitrogen availability in grasslands: the role of plant nitrogen concentration

    (Liesbeth) E.S. Bakker, J.M.H. Knops, D.G. Milchunas, M.E. Ritchie, H. Olff
    Herbivores may influence the nitrogen (N) recycling rates and consequently increase or decrease the productivity of grasslands. Plant N concentration emerged as a critical parameter to explain herbivore effects from several conceptual models, which predict that herbivores decrease soil N availability when plant N concentration is low whereas they increase it when plant N concentration is high (Hobbs 1996, Ritchie et al. 1998, Pastor et al. 2006). However, a broader cross-site comparison among published studies to test these predictions is hampered by the different methodologies used to measure soil N availability or a proxy thereof, and a lack of measurements of plant N concentration. Therefore it remains unclear whether these model predictions are generally valid across a range of grasslands. We tested whether there is a relationship between plant N concentration and herbivore impact on soil N availability (measured with resin bags) with a study of replicate 6–8 year old exclosures (with an unfenced control) of vertebrate herbivores (>1 kg) established at each of seven grassland sites in North America and Europe. Contrary to model predictions, we found a negative relationship between the effect of herbivores on resin bag soil N availability and plant N concentration. Our study confir
  • Basic and Applied Ecology

    Contrasting effects of large herbivore grazing on smaller herbivores

    (Liesbeth) E.S. Bakker, H. Olff, J.M. Gleichman
    Assemblages of large herbivores may compete for food or facilitate one another. However, small vertebrate herbivore species co-occurring with large herbivores may be affected by large herbivore grazing through changes in plant species composition, nutrient content and vegetation structure. These changes can be either positive or negative for the smaller herbivores, but this may depend on the species of small herbivores. We experimentally tested the impact of cattle grazing on habitat choice of European rabbits (Oryctolagus cuniculus) and common voles (Microtus arvalis). We excluded cattle for 7 years and measured changes in vegetation parameters, and the response of rabbits and voles. Rabbits were facilitated by cattle, whereas voles strongly preferred vegetation without cattle. The facilitation effect was stronger at low rabbit densities. Vegetation biomass and nitrogen concentration were not affected by cattle grazing, but vegetation height increased significantly where cattle were excluded. Plant species composition also changed following cattle exclusion; however, the main food plants of rabbits and voles remained abundant in each grazing treatment. We conclude that the response of both rabbits and voles predominantly reflect the differences in vegetation height in the presence and absence of cattle, but in a contrasting fashion. The difference in response between rabbits and voles may result from reduced perceived predation risk, which is lowest in high vegetation for voles, but in short vegetation for rabbits, which depend on their burrows for safety. The use of large herbivores in grassland conservation management can thus have a contrasting effect on different species of small herbivores.
  • Ecology Letters

    Herbivore impact on grassland plant diversity depends on habitat productivity and herbivore size

    (Liesbeth) E.S. Bakker, M.E. Ritchie, H. Olff, D.G. Milchunas, J.M.H. Knops
    Mammalian herbivores can have pronounced effects on plant diversity but are currently declining in many productive ecosystems through direct extirpation, habitat loss and fragmentation, while being simultaneously introduced as livestock in other, often unproductive, ecosystems that lacked such species during recent evolutionary times. The biodiversity consequences of these changes are still poorly understood. We experimentally separated the effects of primary productivity and herbivores of different body size on plant species richness across a 10-fold productivity gradient using a 7-year field experiment at seven grassland sites in North America and Europe. We show that assemblages including large herbivores increased plant diversity at higher productivity but decreased diversity at low productivity, while small herbivores did not have consistent effects along the productivity gradient. The recognition of these large-scale, cross-site patterns in herbivore effects is important for the development of appropriate biodiversity conservation strategies. [KEYWORDS: Cross-site ; fertility ; grazing ; plant–animal ;species richness]
  • Journal of Applied Ecology

    Ecological anachronisms in the recruitment of temperate light-demanding tree species in wooded pastures

    (Liesbeth) E.S. Bakker, Han Olff, C. Vandenberghe, K. de Maeyer, R. Smit, J.M. Gleichman, F.W.M. Vera
    1. Light-demanding trees and thorny shrubs in temperate plant communities may reflect adaptations to now-extinct large grazers, such as aurochs and tarpans, rendering these adaptations ecological anachronisms. 2. We explored the ecological functions of plant traits of Quercus robur and Prunus spinosa in areas grazed by cattle and horses, the domesticated descendants of aurochs and tarpans. Specifically, we tested the hypothesis that grazing induces a shifting mosaic of grassland, shrub thickets and woodlands through the key process of associational resistance: the protection of palatable young trees by thorny shrubs. 3. An exclosure experiment with transplanted Q. robur seedlings revealed that Q. robur grew best in grassland exclosures and on the edge of thorny shrub thickets, which may be viewed as an optimal balance between sufficient protection from large herbivores and sufficient light availability. 4. A cross-site comparison of four floodplain woodlands in north-western Europe showed that Q. robur can regenerate in the presence of large herbivores through spatial association with P. spinosa. However, we found that expansion of P. spinosa shrubs and Q. robur coincided with periods of low rabbit abundance and not with livestock density. From this, it appears that the process of associational resistance does not work with rabbits. 5. Synthesis and applications. With extensive grazing by large (domesticated) grazers in temperate floodplains, a shifting mosaic of grassland, shrubs and trees may develop that has high conservation value. Palatable, light-demanding Q. robur seedlings can successfully regenerate in spiny P. spinosa shrubs through associational resistance. This process does not offer protection from abundant small herbivores, such as rabbits, that can inhibit the recruitment of shrubs and trees in this mosaic vegetation. In floodplain meadows frequent flooding may be an efficient way to reduce rabbit populations, with dry conditions in summer and wet in winter. When floodplain meadows are combined with adjacent higher grounds, large herbivores can escape the floods through migration.
  • Ecology

    Spatial heterogeneity, not visitation bias, dominates variation in herbivory: Reply

    S.M. Louda, A.M. Parkhurst, K.L. Bradley, (Liesbeth) E.S. Bakker, J.M.H. Knops, E.I. Damschen, L.M. Young
  • Oecologia

    Impact of herbivores on nitrogen cycling: contrasting effects of small and large species

    (Liesbeth) E.S. Bakker, Han Olff, M. Boekhoff, J.M. Gleichman, Frank Berendse
    Herbivores are reported to slow down as well as enhance nutrient cycling in grasslands. These conflicting results may be explained by differences in herbivore type. In this study we focus on herbivore body size as a factor that causes differences in herbivore effects on N cycling. We used an exclosure set-up in a floodplain grassland grazed by cattle, rabbits and common voles, where we subsequently excluded cattle and rabbits. Exclusion of cattle lead to an increase in vole numbers and a 1.5-fold increase in net annual N mineralization at similar herbivore densities (corrected to metabolic weight). Timing and height of the mineralization peak in spring was the same in all treatments, but mineralization in the vole-grazed treatment showed a peak in autumn, when mineralization had already declined under cattle grazing. This mineralization peak in autumn coincides with a peak in vole density and high levels of N input through vole faeces at a fine-scale distribution, whereas under cattle grazing only a few patches receive all N and most experience net nutrient removal. The other parameters that we measured, which include potential N mineralization rates measured under standardized laboratory conditions and soil parameters, plant biomass and plant nutrient content measured in the field, were the same for all three grazing treatments and could therefore not cause the observed difference. When cows were excluded, more litter accumulated in the vegetation. The formation of this litter layer may have added to the higher mineralization rates under vole grazing, through enhanced nutrient return through litter or through modification of microclimate. We conclude that different-sized herbivores have different effects on N cycling within the same habitat. Exclusion of large herbivores resulted in increased N annual mineralization under small herbivore grazing.
  • Journal of Vegetation Science

    Impact of different-sized herbivores on recruitment opportunities for subordinate herbs in grasslands

    Potential effects of herbivores on plant species diversity depend on herbivore size, species and density. In this study we examine the effect of different-sized herbivores (cattle and rabbits) on recruitment of subordinate herbs in grasslands. We show that in a grazed floodplain, grassland plant species richness is mainly determined by the presence of many species of subordinate herbs. These herbs experience high colonization and extinction rates. We conclude that the creation of colonization opportunities for subordinate herbs plays a crucial role in maintaining plant species richness in productive grasslands. We found that cattle disperse large amounts of seeds via their dung, over ten times more than rabbits. Rabbits create more and on average larger bare soil patches than cattle. In a field experiment artificial disturbances improved germination success tremendously for four tested herb species. We found that bare soil is the best regeneration site, while cattle dung gave a too strong nutrient stimulus, resulting in tall vegetation and therefore light limitation. These results can be confirmed with results from field monitoring plots where plant species richness was positively related to the occurrence of bare soil patches. Therefore both large and small herbivores have a major impact on dispersal and colonization, but for different reasons. Cattle are identified as most important for seed dispersal whereas rabbits have a main effect as creators of disturbances. These results emphasize the importance of distinguishing between herbivore species in assessing their (potential) effects.
  • Ardea

    Exploitation of a new staging area in the Dutch Wadden Sea by Greylag Geese Anser anser: the importance of food-plant dynamics

    (Liesbeth) E.S. Bakker, R. Van der Wal, P. Esselink, M.A.M. Siepel
    The colonisation by Greylag Geese Anser anser of a new autumn migration staging area was studied on the island of Schiermonnikoog, The Netherlands. Over 500 Greylag Geese first visited the island in 1991. During subsequent years, peak numbers rose to 700-900 birds. The geese most likely originated from the neighbouring staging area on the mainland, the Lauwersmeer, where goose numbers had levelled off since 1985. Because of the time-lag between saturation of the source population and colonisation of the island, changes on the island itself were investigated as a possible trigger for the arrival of the geese. Potential food availability on the island had increased for the geese as a result of vegetation succession. Two food-plants, Sea Club-rush Scirpus maritimus and Common Cord-grass Spartina anglica have increased over the last four decades. Greylag Geese fed mostly on Scirpus tubers and Spartina rhizomes. The soluble-carbohydrate content of the latter two food items did not differ significantly, and was approximately 25% on a dry weight basis. Negative effects of grubbing by Greylag Geese on stands of both Scirpus and Spartina appeared limited during the study period. Although Greylag Geese now spend most of the year in agricultural areas, our study indicates that natural habitats are still of importance for migrating Greylag Geese as staging areas.
  • Plant Biology

    Shifting mosaics in grazed woodlands driven by the alternation of plant facilitation and competition

    Han Olff, F.W.M. Vera, J. Bokdam, (Liesbeth) E.S. Bakker, J.M. Gleichman, K. de Maeyer, R. Smit
    Free-ranging large grazers, such as cattle and horses, are increasingly reintroduced to former agricultural areas in Western Europe in order to restore natural and diverse habitats. In this review we outline mechanisms by which large grazers induce and maintain structural diversity in the vegetation (mosaics of grasslands, shrub thickets and trees). This variation in vegetation structure is considered to be important for the conservation of biodiversity of various plant and animal groups. The process of spatial association with unpalatable plants (associational resistance) enables palatable plants to establish in grasslands maintained by large grazers. In this way, short unattractive (thorny, low quality or toxic) species facilitate taller unattractive shrubs, which facilitate palatable trees, which in turn outshade the species that facilitated their recruitment. Established trees can, therefore, not regenerate under their own canopy, leading to cyclic patch dynamics. Since this cyclic dynamic occurs on a local scale, this contributes to shifting mosaics. The mechanisms involved in creating and maintaining the resulting shifting mosaics are described for temperate floodplain and heathland ecosystems, including the effects on nutrient transport within grazed landscapes. How grazing leads to shifting mosaics is described in terms of plant functional types, allowing potential generalisation to other ecosystems. The resulting interaction web of grasses, unpalatable forbs and shrubs, palatable light-demanding trees and shade-tolerant trees is discussed, and was found to contain various interesting direct and indirect effects. The key process contributing to spatial diversity in vegetation structure is the alternation of positive (facilitation) interactions between plant species at one life cycle stage, and competitive displacement at another stage. Crazing thus causes directional successional sequences to change to shifting mosaics. The implications of this theory for nature conservation are discussed, including the relevant management problems, possible choices and practical solutions. We conclude that the theoretical framework outlined in this review provides helpful insights when coping with nature conservation issues in temperate woodland habitats.
  • Journal of Vegetation Science

    Soil seed bank composition along a gradient from dry alvar grassland to Juniperus shrubland

    Jan P. Bakker, (Liesbeth) E.S. Bakker, E. Rosen, G.L. Verweij, R.M. Bekker
    Dry alvar grasslands on limestone on the Baltic island of Oland, SE Sweden, are very species-rich as long as the traditional agricultural exploitation of grazing and fire wood collection continues. After abandonment, encroachment of Juniperus communis starts and a closed woodland can develop within 100 yr. A chronosequence, representing a successional series, was used for the comparison of sites still grazed, and sites ungrazed for about 20, 55 and 80 yr, respectively. Out of the 58 characteristic dry alvar grassland species 55 % disappeared from the established vegetation after 80 yr of abandoning, and 80 % also vanished from the seed bank. Arenaria serpyllifolia, Trifolium repens, Agrostis vinealis, Linum catharticum, Polygala vulgaris, Cerastium fontanum, Luzula campestris, Achillea millefolium and Potentilla tabernaemontani were the only species left in the seed bank. More than 75 % of the dry alvar grassland species were classified as having a transient or short-term persistent seed bank. It is concluded that restoration management, by cutting junipers, of overgrown dry alvar grassland cannot rely on the longevity of seeds in the soil. Seeds have to be dispersed by wind or grazing animals.

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