Casper van Leeuwen

Dr. Casper van Leeuwen

Postdoc

Bezoekadres

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands

Over

Ecologist studying species movement and species interactions in aquatic ecosystems. I aim to understand how, why and when organisms move – and how this movement structures food webs, populations and communities.

Biografie

I study the movement and interactions of plants and animals in freshwater ecosystems, with the aim to understand how, why and when organisms move – and how their consequential presence or absence affects other organisms in aquatic food webs. Freshwater ponds, lakes and rivers are suitable systems for studying movement because they are often linear (river systems) or isolated by land (ponds and lakes). I integrate studies on multiple tropic levels, including phytoplankton, zooplankton, aquatic invertebrates, plants, fish and waterbirds. How and why do organisms move through these challenging landscapes, how do they colonize and invade new areas, and how do they interact with other species to form communities and structured food webs? I study these questions on both ecological and evolutionary time scales, with applicability towards conservation and restoration.

More information can be found on www.caspervanleeuwen.info

Onderzoeksgroepen

CV

Nevenfuncties

Publicaties

Peer-reviewed publicaties

  • Freshwater Biology
    28-02-2023

    Cover Image

    Andy J. Green, Ádám Lovas‐Kiss, Chevonne Reynolds, Esther Sebastián‐González, Giliandro G. Silva, Casper van Leeuwen, David M. Wilkinson
    https://doi.org/10.1111/fwb.13929
  • Freshwater Biology
    31-01-2023

    Dispersal of aquatic and terrestrial organisms by waterbirds

    Andy J. Green, Adam Lovas-Kiss, Chevonne Reynolds, Esther Sebastián‐González, Giliandro G. Silva, Casper van Leeuwen, David M. Wilkinson

    We review progress in our understanding of the importance of waterbirds as dispersal vectors of other organisms, and identify priorities for further research.
    Waterbirds are excellent for long-distance dispersal (LDD), whereas other vectors such as fish and mammals disperse similar propagules, but over shorter distances. Empirical studies of internal and external transport by waterbirds have shown that the former mechanism generally is more important. Internal transport is widely recognised for aquatic plants and aquatic invertebrates with resting eggs, but also is important for other organisms (e.g., terrestrial flowering plants not dispersed by frugivores, bryophytes, tardigrades, fish eggs).
    Waterbird vectors also are important in terrestrial habitats, and provide connectivity across terrestrial–aquatic boundaries. There are important differences in the roles of different waterbird species, especially those using different habitats along the aquatic–terrestrial gradient. Early attempts to predict zoochory based on propagule morphology have been found wanting, and more research is needed into how the traits of vectors and vectored organisms (including life history, dormancy and growth traits) explain dispersal interactions. Experimental studies have focused on the potential of propagules to survive internal or external transport, and research into factors determining the establishment success of propagules after dispersal is lacking.
    Recent spatially explicit models of seed dispersal by waterbirds should be expanded to include invertebrate dispersal, and to compare multiple bird species in the same landscape. Network approaches have been applied to plant–waterbird dispersal interactions, and these are needed for invertebrates. Genetic studies support effective LDD of plants and invertebrates along waterbird flyways, but there remains a lack of examples at a local scale. Next Generation Sequencing and genomics should be applied to waterbird-mediated dispersal across the landscape. More studies of biogeography, community ecology, or population genetics should integrate waterbird movements at the design stage.
    Zoochory research has paid little attention to the dispersal of non-pathogenic microbes (both eukaryotic and prokaryotic). Nevertheless, there is evidence that dispersal via avian guts can be central to the connectivity of aquatic microbial metacommunities. More work on microbial dispersal by waterbirds should explore its implications for biogeochemistry, and the interchange with gut flora of other aquatic organisms. In the Anthropocene, the role of migratory waterbirds in LDD of plants and other organisms is particularly important, for example in compensating for loss of large migratory mammals and fish, allowing native species to adjust their distributions under global warming, and spreading alien species along flyways after their initial introductions by human vectors. Recent technological advances have opened exciting opportunities that should be fully exploited to further our understanding of dispersal by waterbirds.
    https://doi.org/10.1111/fwb.14038
  • Ecography
    01-2023

    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.
    https://doi.org/10.1111/ecog.06470
  • Science of the Total Environment
    2022

    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.
    https://doi.org/10.1016/j.scitotenv.2021.152156
  • Ecological Engineering
    2022

    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, Valérie C. 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.

    https://doi.org/10.1016/j.ecoleng.2021.106474
  • Freshwater Biology
    2022

    A predatory waterbird as a vector of plant seeds and aquatic invertebrates

    Maria J. Navarro-Ramos, Andy J. Green, Adam Lovas-Kiss, Jacinto Roman, Kane Brides, Casper van Leeuwen

    Omnivorous waterbirds play an important role in aquatic ecosystems as dispersal vectors via direct ingestion, transportation, and egestion of plant and invertebrate propagules (i.e. endozoochory). Predatory birds also have the potential to disperse plants and invertebrates that were first carried internally or externally by their prey animals. However, the potential contribution of predatory waterbird species to propagule dispersal in aquatic ecosystems remains understudied. We chose the grey heron Ardea cinerea (Ardeidae) to study the potential of predatory waterbirds to disperse propagules within and among aquatic ecosystems. We hypothesised that: (1) herons disperse a wide variety of plant and invertebrate propagules, from different habitats, with different morphologies (i.e. dispersal syndromes), and including both native and alien species; (2) propagules are ingested with prey species that are primary dispersal vectors (i.e., herons are secondary dispersers); (3) heron pellets show a similar abundance and richness of propagules across their widespread range. We collected 73 regurgitated heron pellets containing undigestible remains from 12 locations across the U.K. and The Netherlands, and examined the taxonomic diversity of plant seeds, invertebrates and prey remains. Pellets were dominated by mammal hairs (99% by volume), and bones confirmed the ingestion of small mammals (prevalence of 38%, e.g. water voles Arvicola amphibius), fish (14%), and birds or amphibians (6%). A total of 266 intact plant seeds were recovered from 71% of the pellets, representing 50 taxa from 17 plant families, including the alien Cotula coronopifolia. The cumulative number of plant species dispersed was lower at higher latitudes. Eight plant species recorded had not previously been recorded as dispersed via waterbirds, and only three species have an endozoochorous dispersal syndrome. Plant taxa were dominated by Caryophyllaceae, Cyperaceae, Juncaceae, and Poaceae, with 24 species from the littoral zone (Ellenberg moisture values of 7–12) and 21 terrestrial species (Ellenberg moisture values of 4–6). Intact invertebrate propagules were found in 30% of the pellets, dominated by Cladocera (Daphniidae) and Bryozoa (including the alien Plumatella casmiana). Our results demonstrate that grey herons disperse plant seeds and aquatic invertebrates widely in north-western Europe. Herons regurgitate pellets that contain plant and invertebrate propagules from both aquatic or terrestrial habitats, for which secondary dispersal via ingestion along with prey is the likely underlying mechanism (i.e. propagules either attached to or in the digestive systems of the various prey). Our findings showcase the potential of predatory waterbirds as vectors of plants and invertebrates, and how they may facilitate connectivity between freshwater and terrestrial habitats.

    https://doi.org/10.1111/fwb.13870
  • Oikos
    2022

    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.
    https://doi.org/10.1111/oik.09254
  • Freshwater Biology
    2022

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

    Hui Jin, Casper van Leeuwen, Ralph J.M. Temmink, (Liesbeth) E.S. Bakker

    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.

    https://doi.org/10.1111/fwb.13904
  • Journal of Ecology
    2021

    Spatial patterns of weed dispersal by wintering gulls within and beyond an agricultural landscape

    V. Martín Vélez, Casper van Leeuwen, M. Sanchez, F. Hortas, J. Shamoun-Baranes, C Thaxter, L. Lens, C Camphuysen, A.J. Green
    Non-frugivorous waterbirds disperse a wide variety of plants by endozoochory, providing longer-dispersal distances than other mechanisms. Many waterbirds visit both agricultural and natural landscapes during their daily movements, but potential bird-mediated dispersal of weed plants within and from agricultural landscapes to other habitats is commonly overlooked. Gulls (Laridae) are expanding in numbers and increasingly exploiting anthropogenic habitats worldwide, with possible growing implications for the spread of weeds. Yet, to date, there are no studies on the spatial distribution of weed dispersal by waterbirds. We developed a plant dispersal model based on movements of 19 Larus fuscus using ricefields, via GPS telemetry. We combined daily movements with two curves estimating the retention times of plant seeds in their guts: (a) an experimental curve based on retention time in captivity for four weeds with dry fruits known to be dispersed by gulls: Juncus bufonius, Cyperus difformis, Polypogon monspeliensis and the alien Amaranthus retroflexus; (b) a theoretical curve based on the interspecific scaling relationship between body mass and mean retention time. Median dispersal distances of weed plant seeds by gulls ranged between 690 and 940 m, but maximum distances exceeded 150 km. The theoretical retention time model showed higher median dispersal distances than the experimental retention time model. Spatial patterns of weed deposition were very similar between retention time methods, and most strongly depended on gull movements. Variation between individual gulls had little influence on seed shadows. About 92% of all seeds (>10,000 intact seeds per day) were dispersed within the ricefield area of 370 km2. The remaining 8% of seeds were deposited beyond ricefields into other habitats, 42% of which reached moist environments (other irrigated agriculture, rivers and natural wetlands) presumably suitable for weed establishment. Synthesis. Gulls can disperse weed plants over long distances across a mosaic of habitats. This implies exchange of weed plant species between human-dominated and natural areas by waterbirds as dispersal vectors. This spatial study highlights the importance of non-frugivorous birds for long-distance plant dispersal, which is generally an overlooked mechanism in studies aiming to predict and manage expansion of weed plants.
    https://doi.org/10.1111/1365-2745.13619
  • Ecological Solutions and Evidence
    2021

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

    Casper van Leeuwen, Ralph Temmink, Hui Jin, Y Kahlert, B.J.M. Robroek, M.P. Berg, L.P.M. Lamers, Marloes van den Akker, R. Posthoorn, A. Boosten, Han Olff, (Liesbeth) E.S. Bakker
    https://doi.org/10.1002/2688-8319.12098
  • Oikos
    07-2020

    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.
    https://doi.org/10.1111/oik.07082
  • Journal of Ecology
    07-2020

    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.
    https://doi.org/10.1111/1365-2745.13380
  • Scientific Reports
    2020

    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
    https://doi.org/10.1038/s41598-020-62660-1
  • Frontiers in Ecology and Evolution
    2020

    Animal-Mediated Dispersal in Understudied Systems

  • Science of the Total Environment
    2020

    Functional connectivity network between terrestrial and aquatic habitats by a generalist waterbird, and implications for biovectoring

    Víctor Martín-Vélez, B. Mohring, Casper van Leeuwen, J. Shamoun-Baranes, C.B. Thaxter, J.M. Baert, C.J. Camphuysen, A.J. Green
    https://doi.org/10.1016/j.scitotenv.2019.135886
  • Frontiers in Plant Science
    08-01-2019

    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.
    https://doi.org/10.3389/fpls.2018.01947
  • Journal of Applied Ecology
    2019

    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.
    https://doi.org/10.1111/1365-2664.13256
  • PLoS One
    20-09-2018

    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.
    https://doi.org/10.1371/journal.pone.0204116
  • Frontiers in Plant Science
    2018

    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.
    https://doi.org/10.3389/fpls.2018.00134
  • Frontiers in Plant Science
    2018

    Internal and external dispersal of plants by animals: an aquatic perspective on alien interference

    Many alien plants use animal vectors for dispersal of their diaspores (zoochory). If alien plants interact with native disperser animals, this can interfere with animal-mediated dispersal of native diaspores. Interference by alien species is known for frugivorous animals dispersing fruits of terrestrial plants by ingestion, transport and egestion (endozoochory). However, less attention has been paid to possible interference of alien plants with dispersal of diaspores via external attachment (ectozoochory, epizoochory or exozoochory), interference in aquatic ecosystems, or positive effects of alien species on dispersal of native plants. This literature study addresses the following hypotheses: (1) alien plants may interfere with both internal and external animal-mediated dispersal of native diaspores; (2) interference also occurs in aquatic ecosystems; (3) interference of alien plants can have both negative and positive effects on native plants. The studied literature revealed that alien species can comprise large proportions of both internally and externally transported diaspores. Because animals have limited space for ingested and adhering diaspores, alien species affect both internal and external transport of native diaspores. Alien plant species also form large proportions of all dispersed diaspores in aquatic systems and interfere with dispersal of native aquatic plants. Alien interference can be either negative (e.g. through competition with native plants) or positive (e.g. increased abundance of native dispersers, changed disperser behavior or attracting additional disperser species). I propose many future research directions, because understanding whether alien plant species disrupt or facilitate animal-mediated dispersal of native plants is crucial for targeted conservation of invaded (aquatic) plant communities.
    https://doi.org/10.3389/FPLS.2018.00153
  • Environmental Impact Assessment Review
    07-2017

    Environmental risk assessment for invasive alien species: A case study of apple snails affecting ecosystem services in Europe

    Gianni Gilioli, Gritta Schrader, Nils Carlsson, Ellen Van Donk, Casper van Leeuwen, Pablo R. Martín, Sara Pasquali, Montserrat Vilà, Sybren Vos
    Abstract The assessment of the risk posed by invasive alien species (IAS) to the environment is a component of increasing importance for Pest Risk Analysis. Standardized and comprehensive procedures to assess their impacts on ecosystem services have been developed only recently. The invasive apple snails (Pomacea canaliculata and P. maculata) are used as a case study to demonstrate the application of an innovative procedure assessing the potential impact of these species on shallow freshwater ecosystems with aquatic macrophytes in Europe. The apple snail, Pomacea maculata, recently established in the Ebro delta in Spain resulting in a serious threat to rice production and wetlands, having also a high risk to spread to other European wetlands. Here, the population abundance of apple snails is regarded as the main driver of ecosystem change. The effects of ecosystem resistance, resilience and pest management on snail population abundance are estimated for the short (5 years) and the long (30 years) term. Expert judgment was used to evaluate the impacts on selected ecosystem services in a worst-case scenario. Our study shows that the combined effects of apple snails are estimated to have profound effects on the ecosystem services provided by shallow, macrophyte-dominated ecosystems in Europe. This case study illustrates that quantitative estimates of environmental impacts from different IAS are feasible and useful for decision-makers and invasive species managers that have to balance costs of control efforts against environmental and economic impacts of invasive species.
    https://doi.org/10.1016/j.eiar.2017.03.008
  • Biology Letters
    2017

    Great cormorants reveal overlooked secondary dispersal of plants and invertebrates by piscivorous waterbirds

    Casper van Leeuwen, A. Lovas-Kiss, M. Ovegård, Andy J. Green
    In wetland ecosystems, birds and fish are important dispersal vectors for plants and invertebrates, but the consequences of their interactions as vectors are unknown. Darwin suggested that piscivorous birds carry out secondary dispersal of seeds and invertebrates via predation on fish. We tested this hypothesis in the great cormorant (Phalacrocorax carbo L.). Cormorants regurgitate pellets daily, which we collected at seven European locations and examined for intact propagules. One-third of pellets contained at least one intact plant seed, with seeds from 16 families covering a broad range of freshwater, marine and terrestrial habitats. Of 21 plant species, only two have an endozoochory dispersal syndrome, compared with five for water and eight for unassisted dispersal syndromes. One-fifth of the pellets contained at least one intact propagule of aquatic invertebrates from seven taxa. Secondary dispersal by piscivorous birds may be vital to maintain connectivity in meta-populations and between river catchments, and in the movement of plants and invertebrates in response to climate change. Secondary dispersal pathways associated with complex food webs must be studied in detail if we are to understand species movements in a changing world.
    https://doi.org/10.1098/rsbl.2017.0406
  • Functional Ecology
    2016

    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.
    https://doi.org/10.1111/1365-2435.12485
  • Freshwater Biology
    2015

    Internal transport of alien and native plants by geese and ducks: an experimental study

    Alberto Garcia-Alvarez, Casper van Leeuwen, Carlos J. Luque, Andreas Hussner, Alberto Velez-Martin, Andres Perez-Vazquez, Andy J. Green, Eloy M. Castellanos
    Alien plant species are rapidly spreading in aquatic ecosystems around the world, causing major ecological effects. They are typically introduced by humans, after which natural vectors facilitate their further spread. Migratory waterbirds have long been recognised as important dispersal vectors for native and aquatic plants, yet little is known about their role in the spread of alien species. We determined experimentally the potential for long-distance dispersal of native and alien wetland plants in Europe by two abundant waterfowl: mallards Anas platyrhynchos and greylag geese Anser anser. We fed seeds from two plants alien to Europe and two native plants to 10 individuals of each bird species, testing for the effects of bird and plant species on the potential for dispersal. Intact seeds were retrieved from faeces for up to 4days after ingestion. The proportion of seeds retrieved intact varied significantly between plant, but not bird, species. Retrieval was highest for the invasive water primrose Ludwigia grandiflora (>35% of ingested seeds), lowest for the invasive cordgrass Spartina densiflora (<3%) and intermediate for the native glasswort Arthrocnemum macrostachyum and seablite Suaeda vera (5-10%). Seed retrieval patterns over time varied between both plant and bird species. Contrary to expectations, seeds were retained in the gut for longer in the smaller mallards. No Spartina seeds germinated after retention for over 8h, whereas some seeds of the other species germinated even after retention for 72h. Germinability was reduced by gut passage for Ludwigia and Arthrocnemum seeds. Ludwigia seeds recovered from geese were more likely to germinate than those recovered from mallards. Time to germination was reduced by gut passage for Spartina and Ludwigia, but increased with retention time. Ducks and geese evidently have the potential for long-distance transport of alien and native plant seeds, with maximal dispersal distances of well over 1000km. The much greater potential of Ludwigia than Spartina for dispersal by waterfowl is consistent with its faster expansion across Europe. Maximum retention times of wetland seeds have been underestimated in previous experimental studies that lasted only 1-2days. Contrary to previous studies, wetland plants with large seeds, such as Ludwigia, can still show high potential for long-distance dispersal. More attention should be paid to the role of waterbirds as vectors of alien plants and to the role of migratory geese as vectors of plants in general.
    https://doi.org/10.1111/fwb.12567
  • Aquatic Botany
    2015

    Regurgitation by waterfowl: an overlooked mechanism for long-distance dispersal of wetland plant seeds?

    Erik Kleyheeg, Casper van Leeuwen
    Abstract Birds commonly regurgitate indigested particles after foraging. Many frugivorous birds regurgitate seeds ingested with the flesh of fruits, which importantly contributes to plant dispersal in terrestrial ecosystems. In freshwater ecosystems, waterbirds are known to defecate viable seeds in their faeces, but little is known about regurgitation as a potential additional seed dispersal mechanism. We experimentally fed eight mallards (Anas platyrhynchos) with a high and low volume of seeds of ten wetland plant species, and monitored regurgitation and defecation of intact seeds over 24 h. Regurgitation occurred at least once in all individual mallards and was induced by two different mechanisms: i) feeding of high food volumes was significantly associated with regurgitation of all seed species from the crop after retention times of 1-3 h, and ii) large indigestible seeds were expelled from the gizzard 11 or more hours after feeding. Seed regurgitation was much less plant species-specific than survival of seeds passing digestion, which suggests it is a particularly suitable dispersal mechanism for plant species unable to disperse by endozoochory (such as plant species with large, soft-bodied seeds). Observations of regurgitation by wild waterbirds are needed to improve our knowledge on this additional role of waterbirds in ecosystem functioning.
    https://doi.org/10.1016/j.aquabot.2015.06.009
  • Oikos
    2015

    Bird-mediated seed dispersal: reduced digestive efficiency in active birds modulates dispersal capacity of plant seeds

    Erik Kleyheeg, Casper van Leeuwen, M.A. Morison, Bart A. Nolet, Merel Soons
    Plant populations in fragmented ecosystems rely largely on internal dispersal by animals. To unravel the mechanisms underlying this mode of dispersal, an increasing number of experimental feeding studies is carried out. However, while physical activity is known to affect vertebrate digestive processes, almost all current knowledge on mechanisms of internal seed dispersal has been obtained from experiments with resting animals. We investigated how physical activity of the mallard (Anas platyrhynchos), probably the quantitatively most important biotic dispersal agent in aquatic habitats in the entire Northern Hemisphere, affects gut passage survival and retention time of ingested plant seeds. We fed seeds of nine common wetland plants to mallards trained to subsequently swim for 6 hours in a flume tank at different swimming speeds (activity levels). We compared gut passage survival and retention times of seeds against a control treatment with mallards resting in a conventional dry cage. Intact gut passage of seeds increased significantly with mallard activity (up to 80% in the fastest swimming treatment compared to the control), identifying reduced digestive efficiency due to increased metabolic rates as a mechanism enhancing the dispersal potential of ingested seeds. Gut passage speed was modestly accelerated (13% on average) by increased mallard activity, an effect partly obscured by the interaction between seed retention time and probability of digestion. Gut passage acceleration will be more pronounced in digestion-resilient seed species, thereby modulating their dispersal distances. Our findings imply that seed dispersal potential by mallards calculated from previous experiments with resting birds is highly underestimated, while dispersal distances may be overestimated for some plant species. Similar effects of physical activity on digestive efficiency of mammals suggests that endozoochorous dispersal of plant seeds by vertebrates is more effective and plays a quantitatively more important ecological role in both terrestrial and aquatic ecosystems than previously thought.
    https://doi.org/10.1111/oik.01894
  • Journal of Ecology
    2014

    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.
    https://doi.org/10.1111/1365-2745.12250
  • Freshwater Biology
    2013

    How did this snail get here? Several dispersal vectors inferred for an aquatic invasive species

    Casper van Leeuwen, Naomi Huig, G. Van der Velde, T. Van Alen, C.A.M. Wagemaker, C.D.H. Sherman, M.R.J. Klaassen, J. Figuerola
    How species reach and persist in isolated habitats remains an open question in many cases, especially for rapidly spreading invasive species. This is particularly true for temporary freshwater ponds, which can be remote and may dry out annually, but may still harbour high biodiversity. Persistence in such habitats depends on recurrent colonisation or species survival capacity, and ponds therefore provide an ideal system to investigate dispersal and connectivity. 2. Here, we test the hypothesis that the wide distributions and invasive potential of aquatic snails is due to their ability to exploit several dispersal vectors in different landscapes. We explored the population structure of Physa acuta (recent synonyms: Haitia acuta, Physella acuta, Pulmonata: Gastropoda), an invasive aquatic snail originating from North America, but established in temporary ponds in Donana National Park, southern Spain. In this area, snails face land barriers when attempting to colonise other suitable habitat. 3. Genetic analyses using six microsatellite loci from 271 snails in 21 sites indicated that (i) geographically and hydrologically isolated snail populations in the park were genetically similar to a large snail population in rice fields more than 15 km away; (ii) these isolated ponds showed an isolation-by-distance pattern. This pattern broke down, however, for those ponds visited frequently by large mammals such as cattle, deer and wild boar; (iii) snail populations were panmictic in flooded and hydrologically connected rice fields. 4. These results support the notion that aquatic snails disperse readily by direct water connections in the flooded rice fields, can be carried by waterbirds flying between the rice fields and the park and may disperse between ponds within the park by attaching to large mammals. 5. The potential for aquatic snails such as Physa acuta to exploit several dispersal vectors may contribute to their wide distribution on various continents and their success as invasive species. We suggest that the interaction between different dispersal vectors, their relation to specific habitats and consequences at different geographic scales should be considered both when attempting to control invasive freshwater species and when protecting endangered species.
    https://doi.org/10.1111/fwb.12041
  • Freshwater Science
    2012

    Prerequisites for flying snails: external transport potential of aquatic snails by waterbirds

    Casper van Leeuwen, G. Van der Velde
    The widespread distributions of aquatic species often contrast with their limited ability to disperse by their own propulsion among wetlands isolated by land. Studies of the potential role of water birds as dispersal vectors have been focused mainly on internal transport (endozoochory). However, many anecdotal observations that small species adhere to flying birds also exist (ectozoochory). We addressed the hypothesis that ectozoochory may contribute to the widespread distributions of aquatic snails (Gastropoda) in several experiments. We tested the likelihood that snails would attach to mallards (Anas platyrhynchos) leaving macrophyte vegetation with high densities of 3 snail species. All species tested (Gyraulus albus, Anisus vortex, and Radix balthica) readily attached to the mallards’ bodies. The rate of attachment was proportional to snail density, and the birds’ feathers contained most snails. However, Oof the snails detached when mallards subsequently walked for 3 m. Snails of 12 species attached within minutes to any surroundings available when floating in the water, a result indicating that active crawling onto birds may facilitate dispersal. Snails we attached deliberately to duck bills with mud could remain attached for up to 8 h. We measured desiccation tolerance of 13 common aquatic snail species. Almost all snail species survived 48 h of desiccation at 10 to 20uC. The ability to retain water did not differ between species with an operculum and species that form a mucus layer (epiphragm) in their shell openings. Our experiments indicate that aquatic snails possess a range of prerequisites for successful bird-mediated dispersal, but the capacity of snails (and other propagules) to remain attached during flight and successfully colonize new habitats upon arrival must still be assessed.
    https://doi.org/10.1899/12-023.1
  • Oecologia
    2012

    Vector activity and propagule size affect dispersal potential by vertebrates

    Casper van Leeuwen, M. Tollenaar, M.R.J. Klaassen
    Many small organisms in various life stages can be transported in the digestive system of larger vertebrates, a process known as endozoochory. Potential dispersal distances of these “propagules” are generally calculated after monitoring retrieval in experiments with resting vector animals. We argue that vectors in natural situations will be actively moving during effective transport rather than resting. We here test for the first time how physical activity of a vector animal might affect its dispersal efficiency. We compared digestive characteristics between swimming, wading (i.e. resting in water) and isolation (i.e. resting in a cage) mallards (Anas platyrhynchos). We fed plastic markers and aquatic gastropods, and monitored retrieval and survival of these propagules in the droppings over 24 h. Over a period of 5 h of swimming, mallards excreted 1.5 times more markers than when wading and 2.3 times more markers than isolation birds, the pattern being reversed over the subsequent period of monitoring where all birds were resting. Retention times of markers were shortened for approximately 1 h for swimming, and 0.5 h for wading birds. Shorter retention times imply higher survival of propagules at increased vector activity. However, digestive intensity measured directly by retrieval of snail shells was not a straightforward function of level of activity. Increased marker size had a negative effect on discharge rate. Our experiment indicates that previous estimates of propagule dispersal distances based on resting animals are overestimated, while propagule survival seems underestimated. These findings have implications for the dispersal of invasive species, meta-population structures and long distance colonization events.
    https://doi.org/10.1007/s00442-012-2293-0
  • PLoS One
    2012

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

    Casper van Leeuwen, G. Van der Velde, Bart van Lith, M.R.J. Klaassen
    Many plant seeds and invertebrates can survive passage through the digestive system of birds, which may lead to long distance dispersal (endozoochory) in case of prolonged retention by moving vectors. Endozoochorous dispersal by waterbirds has nowadays been documented for many aquatic plant seeds, algae and dormant life stages of aquatic invertebrates. Anecdotal information indicates that endozoochory is also possible for fully functional, active aquatic organisms, a phenomenon that we here address experimentally using aquatic snails. We fed four species of aquatic snails to mallards (Anas platyrhynchos), and monitored snail retrieval and survival over time. One of the snail species tested was found to survive passage through the digestive tract of mallards as fully functional adults. Hydrobia (Peringia) ulvae survived up to five hours in the digestive tract. This suggests a maximum potential transport distance of up to 300 km may be possible if these snails are taken by flying birds, although the actual dispersal distance greatly depends on additional factors such as the behavior of the vectors. We put forward that more organisms that acquired traits for survival in stochastic environments such as wetlands, but not specifically adapted for endozoochory, may be sufficiently equipped to successfully pass a bird's digestive system. This may be explained by a digestive trade-off in birds, which maximize their net energy intake rate rather than digestive efficiency, since higher efficiency comes with the cost of prolonged retention times and hence reduces food intake. The resulting lower digestive efficiency allows species like aquatic snails, and potentially other fully functional organisms without obvious dispersal adaptations, to be transported internally. Adopting this view, endozoochorous dispersal may be more common than up to now thought.
    https://doi.org/10.1371/journal.pone.0032292
  • Journal of Biogeography
    2012

    Gut travellers: internal dispersal of aquatic organisms by waterfowl

    Casper van Leeuwen, G. Van der Velde, J. Van Groenendael, M.R.J. Klaassen
    Aim Patterns of high biodiversity among less mobile organisms throughout isolated locations suggest that passive dispersal importantly contributes to biodiversity. We examined the contribution of waterbirds to the dispersal of plant seeds and macroinvertebrates between aquatic wetlands. Birds are renowned vectors for seeds of terrestrial plants, but less is known about their role in more dispersal-dependent aquatic systems. We therefore performed a meta-analysis on bird-mediated endozoochorous dispersal of aquatic species. Location Our review included studies that collected data world-wide. Methods We analysed data from 81 peer-reviewed publications on endozoochorous dispersal of aquatic plant seeds and macroinvertebrates by waterbirds. Results In total, 36% of 1581 waterbird droppings collected in the field contained one or more intact propagules, with macroinvertebrates found almost as frequently as plant seeds. Positive droppings contained on average 3.3 intact propagules, of which one-third were viable. In 728 trials from 17 published feeding experiments 24% of the ingested propagules were retrieved intact, with c. 6.5% both viable and intact. As many as 17 species of Anatidae and Rallidae were involved in the dispersal of at least 39 species of macroinvertebrates and seeds from 97 species of plants across a wide taxonomic range. Smaller propagules seemed less affected by digestion than larger ones. We provide a first quantitative model that can be used to estimate waterbird-mediated dispersal of propagules between wetlands. This model indicates that an average waterbird has the potential to disperse five viable propagules after flying more than 100 km, and one additional propagule after flying 300 km. Main conclusions We demonstrate that waterbirds have the potential to transport a wide variety of aquatic plants and animals over several hundreds of kilometres. High survival of propagules might be explained by propagule adaptations or by the digestive adaptations of birds, whereby energy absorption is thought to be maximized rather than assimilation efficiency. Our meta-analysis suggests that waterbirds might contribute significantly to wetland biodiversity around the world, despite several limitations to our current knowledge. We outline avenues for future research to address these knowledge gaps
    https://doi.org/10.1111/jbi.12004
  • The Condor
    2010

    Do Red Knots (Calidris canutus Islandica) routinely skip Iceland during southward migration?

    M. Dietz, B. Spaans, A. Dekinga, M.R.J. Klaassen, Casper van Leeuwen, Theunis Piersma
    Subspecies Calidris canutus islandica of the Red Knot breeds on the arctic tundra of northeastern Canada and northern Greenland and winters along the coasts of northwestern Europe. During northward migration, it stops over in either Iceland or northern Norway. It has been assumed that it does the same during southward migration. Using ratios of stable carbon isotopes (δ13C) in whole blood, blood cells, and plasma, we investigated evidence for a stopover in Iceland en route from the breeding grounds to the Dutch Wadden Sea. With the expected diet (shellfish) and stopover duration at Iceland (12–15 days, maximum 17 days) and the turnover rates of blood cells (15.1 days) and plasma (6.0 days), Red Knots that stopped in Iceland should arrive with a blood (cell) δ13C midway between a tundra (−24.7‰) and a marine value (−14.0‰) and a plasma δ13C approaching the marine value (−15.3‰). However, many adults arriving at the Wadden Sea had δ13C ratios in blood (cells) and plasma below these levels, and some arrived with clear tundra signals in blood cells, suggesting that they skipped Iceland during southward migration. Surprisingly, available data suggest this also to be true for juveniles during their first southward migration. The δ13C signature of second-year birds confirmed that they oversummered in the Wadden Sea. Our findings contradict the largely untested idea that juvenile shorebirds make more stopovers than adults as well as the idea that the migration between the Nearctic and Europe is necessarily a two-leg process.
    https://doi.org/10.1525/cond.2010.090139
  • Journal of Animal Ecology
    2007

    Prior knowledge about spatial pattern affects patch assessment rather than movement between patches in tactile-feeding Mallard

    Raymond Klaassen, Bart A. Nolet, Casper van Leeuwen
    1. Heterogeneity in food abundance allows a forager to concentrate foraging effort in patches that are rich in food. This might be problematic when food is cryptic, as the content of patches is unknown prior to foraging. In such case knowledge about the spatial pattern in the distribution of food might be beneficial as this enables a forager to estimate the content of surrounding patches. A forager can benefit from this pre-harvest information about the food distribution by regulating time in patches and/or movement between patches. 2. We conducted an experiment with mallard Anas platyrhynchos foraging in environments with random, regular, and clumped spatial configurations of full and empty patches. An assessment model was used to predict the time in patches for different spatial distributions, in which a mallard is predicted to remain in a patch until its potential intake rate drops to the average intake rate that can be achieved in the environment. A movement model was used to predict lengths of interpatch movements for 3. Consistent with predictions, in the clumped distribution mallard spent less time in an empty patch when the previously visited neighbouring patch had been empty than when it had been full. This effect was not observed for the random distribution. This shows that mallard use pre-harvest information on spatial pattern to improve patch assessment. Patch assessment could not be evaluated for the regular distribution. 4. Movements that started in an empty patch were longer than movements that started in a full patch. Contrary to model predictions this effect was observed for all spatial distributions, rather than for the clumped distribution only. In this experiment mallard did not regulate movement in relation to pattern. 5. An explanation for the result that pre-harvest information on spatial pattern affected patch assessment rather than movement is that mallard move to the nearest patch where the expected intake rate is higher than the critical value, rather than to the patch where the highest intake rate is expected.
    https://doi.org/10.1111/j.1365-2656.2006.01184.x

Projecten & samenwerkingen

Projecten

  • Natuur in Productie: visecologie op de Marker Wadden (NiPFish)

    Project 2019
    Natuur in Productie: visecologie op de Marker Wadden (NiPFish)
    Waterleven
  • Rewilding wetlands

    Project 2016–2024
    Restoring wetlands by allowing water level dynamics and connecting terrestrial and aquatic ecosystems can be considered as a form of aquatic rewilding. Lake restoration project Marker Wadden and the Oostvaardersplassen marsh reset are part of our research program studying the impact of lake and wetland restoration measures on the biodiversity and functioning of aquatic ecosystems.
    limnotron

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