Google Scholar publication overview

 

Deaths among Wild Birds during Highly Pathogenic Avian Influenza A(H5N8) Virus Outbreak, the Netherlands. Kleyheeg et al. (2017) Emerging Infectious Diseases

Abstract: During autumn–winter 2016–2017, highly pathogenic avian influenza A(H5N8) viruses caused mass die-offs among wild birds in the Netherlands. Among the ≈13,600 birds reported dead, most were tufted ducks (Aythya fuligula) and Eurasian wigeons (Anas penelope). Recurrence of avian influenza outbreaks might alter wild bird population dynamics.

URL: https://wwwnc.cdc.gov/eid/article/23/12/17-1086_article

 

Reduction in adverse effects of tracking devices on waterfowl requires better measuring and reporting. Lameris & Kleyheeg (2017) Animal Biotelemetry

Abstract: Since the first studies in the mid-twentieth century, lightweight electronic tracking devices have been increasingly used to study waterfowl movements. With half a century of experience and growing sample sizes, it has become clear that the attachment of a tracking device can affect a bird’s behaviour and fitness. This becomes problematic when it introduces uncertainty about whether the recorded data represent natural behaviour. Waterfowl may be particularly prone to tag effects, since many species are migratory and tracking devices can disrupt their waterproof plumage. The primary aim of this paper is to identify how tracking devices may affect waterfowl survival, migration and reproduction, and how better measuring and reporting of such effects can improve our understanding of the risks, providing a first step towards reducing their impact in future studies. We reviewed literature on electronic tracking of waterfowl to create an overview of currently recognized effects of harness-attached backpacks, implants, subcutaneous attachments and neck collars. Additionally, we analysed developments in the use of attachment methods, the weight of tracking devices relative to bird body mass, and the reporting rate of effects of tracking devices in 202 original tracking studies. We found that although the number of waterfowl tracking studies described in peer-reviewed literature has steeply increased over the past decades, reporting rates of potential effects have decreased from 65.0 to 26.5%. Meanwhile, the mean weight of the tracking devices relative to the bird’s body mass remained stable around 2.0%. Major negative effects were reported in 17% of all studies and were found for all attachment methods. Overall, large differences exist in the occurrence and type of negative effects between species and studies, even if the same tracking methods were used. Inconsistent reporting of effects, lack of control groups to measure effects and incomplete descriptions of the methodology hamper the identification of factors contributing to these effects. To accomplish a reduction in adverse effects of tracking, it is necessary to improve the measuring and reporting of effects. We propose a framework for standardized reporting of methods in primary tracking studies and standardized protocols to measure effects of tracking devices on waterfowl.

URL: http://rdcu.be/xNDE

 

Seed dispersal distributions resulting from landscape-dependent daily movement behaviour of a key vector species. Kleyheeg et al. (2017) Journal of Ecology

Abstract:

  1. Dispersal via animals (zoochory) is a primary mechanism for seed exchange between habitat patches. Recent studies have established that many plant species can survive waterbird gut passage. To quantify the patterns and consequences of waterbird-mediated dispersal, information on ingestion and gut passage must be combined with bird movement data. Such analysis has recently revealed seed dispersal kernels by migrating waterbirds. However, since many waterbird populations are largely resident, and migrating populations spend only a minor part of the main dispersal season (autumn–winter) on active migration, daily regional-scale movements probably cause more frequent dispersal.
  2. We synthesized high-resolution empirical data on landscape-scale movements and seed gut passage times in a key disperser species, the mallard (Anas platyrhynchos), using a spatially explicit, mechanistic model to quantify dispersal distributions resulting from daily autumn–winter movements. We evaluated how landscape composition and seed traits affect these dispersal patterns.
  3. The model indicates that mallards generate highly clumped seed deposition patterns, dispersing seeds primarily between core areas used for foraging and resting. Approximately 34% of all dispersed seeds are transported to communal roost areas, which may function as reservoirs for mallard-dispersed species, and 7% are transported between foraging areas. Landscape-dependent movement patterns strongly affect the dispersal distributions, resulting in multi-modal dispersal kernels, with dispersal distances increasing with fragmentation of freshwater foraging habitat. Seed size-related gut retention times determine the proportion of seeds being dispersed away from the ingestion area, with larger seeds (20 mm3) having a 8–10% higher potential for long-distance dispersal than smaller seeds (0·2 mm3), if surviving gut passage. However, twice as many small seeds will finally accomplish long-distance dispersal due to their higher gut passage survival.
  4. Synthesis. Firstly, this study reveals how seed dispersal patterns resulting from daily waterfowl movements are shaped by landscape-dependent differences in movement patterns. Secondly, seed survival appears more important than retention time in determining the scale of long-distance dispersal by non-migrating mallards. We conclude that the frequent flights of staging waterbirds result in directed dispersal over distances inversely related to wetland availability, indicating that they maintain landscape connectivity across a range from wet to increasingly dry landscapes.

URL: http://onlinelibrary.wiley.com/doi/10.1111/1365-2745.12738/epdf

 

Movement patterns of a keystone waterbird species are highly predictable from landscape configuration. Kleyheeg et al. (2017) Movement Ecology

Abstract:

Background - Movement behaviour is fundamental to the ecology of animals and their interactions with other organisms, and as such contributes to ecosystem dynamics. Waterfowl are key players in ecological processes in wetlands and surrounding habitats through predator-prey interactions and their transportation of nutrients and other organisms. Understanding the drivers of their movement behaviour is crucial to predict how environmental changes affect their role in ecosystem functioning. Mallards (Anas platyrhynchos) are the most abundant duck species worldwide and important dispersers of aquatic invertebrates, plants and pathogens like avian influenza viruses. By GPS tracking of 97 mallards in four landscape types along a gradient of wetland availability, we identified patterns in their daily movement behaviour and quantified potential effects of weather conditions and water availability on the spatial scale of their movements.

Results - We demonstrate that mallard movement patterns were highly predictable, with regular commuting flights at dusk and dawn between a fixed day roost and one or several fixed nocturnal foraging sites, linked strongly to surface water. Wind and precipitation hardly affected movement, but flight distances and home range sizes increased when temperatures dropped towards zero. Flight distances and home range sizes increased exponentially with decreasing availability of freshwater habitat. Total shoreline length and the number of water bodies in the landscape surrounding the roost were the best predictors of the spatial scale of daily mallard movements.

Conclusions - Our results show how mallards may flexibly adjust the spatial scale of their movements to wetland availability in the landscape. This implies that mallards moving between discrete habitat patches continue to preserve biotic connectivity in increasingly fragmented landscapes. The high predictability of mallard movement behaviour in relation to landscape features makes them reliable dispersal vectors for organisms to adapt to, and allows prediction of their ecological role in other landscapes.

URL: https://movementecologyjournal.biomedcentral.com/articles/10.1186/s40462-016-0092-7

 

Seed dispersal potential by wild ducks as estimated from digestive tract analysis. Kleyheeg et al. (2016) Freshwater Biology

Abstract:

  1. Dispersal of plant seeds by ducks and other waterbirds is of great importance to the ecology of freshwater habitats. To unravel the mechanisms of waterbird-mediated seed dispersal, numerous laboratory experiments have been conducted, but effects of seed and waterbird traits on dispersal potential have rarely been investigated under field conditions.
  2. Through analysis of the digestive tracts of 100 wild mallards (Anas platyrhynchos) across a winter season in the Netherlands, we assessed (i) the inter-individual and seasonal variability of seeds in the digestive tract, (ii) the variability of digestive tract organ size and gizzard grit mass, and (iii) the potential effects of seed species traits and gut traits on the survival potential of ingested seeds.
  3. We found 4548 ingested seeds of at least 66 plant species from a wide range of habitats, most of which were retained in the gizzard. Nineteen species had not previously been reported from mallard diets. Individual tracts contained anywhere between 0 and 1048 seeds, of up to 14 species (median of three species). Diet composition and digestive tract size varied substantially between individuals and over the course of the winter season. As predicted from controlled feeding studies, we found that also in wild mallards, size-dependent gut passage survival favours the dispersal of small-seeded species. Despite the large variation in gizzard and small intestine size in this study, their effect on the dispersal potential of ingested seeds in the field remains unclear. We found no difference in dispersal potential between plants species growing in wet or dry habitats.
  4. This study demonstrates that wild mallards are opportunistic seed consumers with a very diverse diet as reflected by seed species composition in both the foregut and hindgut. However, we also show that serious limitations of field-based analyses compared to controlled experiments can impede drawing conclusions about gut passage survival of seeds. The large variability in diet composition among individuals and over time indicates high endozoochorous dispersal potential for a wide range of plant species by wild mallard in aquatic and wetland, as well as surrounding terrestrial habitats.

URL: https://pure.knaw.nl/portal/files/2509984/6150_Kleyheeg.pdf

 

Lack of virological and serological evidence for continued circulation of highly pathogenic avian influenza H5N8 virus in wild birds in the Netherlands, 14 November 2014 to 31 January 2016. Poen et al. (2016) Eurosurveillance

Abstract: In 2014, H5N8 clade 2.3.4.4 highly pathogenic avian influenza (HPAI) viruses of the A/Goose/Guangdong/1/1996 lineage emerged in poultry and wild birds in Asia, Europe and North America. Here, wild birds were extensively investigated in the Netherlands for HPAI H5N8 virus (real-time polymerase chain reaction targeting the matrix and H5 gene) and antibody detection (haemagglutination inhibition and virus neutralisation assays) before, during and after the first virus detection in Europe in late 2014. Between 21 February 2015 and 31 January 2016, 7,337 bird samples were tested for the virus. One HPAI H5N8 virus-infected Eurasian wigeon (Anas penelope) sampled on 25 February 2015 was detected. Serological assays were performed on 1,443 samples, including 149 collected between 2007 and 2013, 945 between 14 November 2014 and 13 May 2015, and 349 between 1 September and 31 December 2015. Antibodies specific for HPAI H5 clade 2.3.4.4 were absent in wild bird sera obtained before 2014 and present in sera collected during and after the HPAI H5N8 emergence in Europe, with antibody incidence declining after the 2014/15 winter. Our results indicate that the HPAI H5N8 virus has not continued to circulate extensively in wild bird populations since the 2014/15 winter and that independent maintenance of the virus in these populations appears unlikely.

URL: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5073202/pdf/eurosurv-21-30349.pdf

 

Going against the flow? A case for upstream dispersal and how to detect uncommon dispersal events. Wubs et al. (2016) Freshwater Biology

Abstract:

  1. Dispersal and colonisation are key processes determining species survival, and their importance is increasing as a consequence of ongoing habitat fragmentation, land-use change and climate change. Identification of long-distance dispersal events, including upstream dispersal, and of the dispersal mechanisms and resulting spatial dispersal patterns involved provides much-needed information for conservation in an era of rapid environmental change.
  2. However, quantifying contemporary dispersal among populations is far from straightforward. We used the relatively well-defined, typically linear, spatial structure of streams, rivers and their associated riparian and aquatic plant populations to illustrate this. We performed a literature review on studies where dispersal and its directionality (upstream versus downstream) were explicitly quantified.
  3. Upstream dispersal was detected in the majority (75%) of examined stream and riparian plant species and mediated mainly by waterfowl, but also by other animals and wind. However, upstream movements are generally less frequent than downstream. Upstream dispersal can occur in excess of tens and sometimes even hundreds of kilometres.
  4. Most of the reviewed studies suffer from important methodological limitations that generate difficulties in detecting uncommon dispersal events. Major limitations include use of molecular ecological analyses based on unrealistic assumptions, and the inability to separate seed from pollen flow. On the basis of these findings, we outline a flexible research design using DNA-based assignment methods that allows quantification of contemporary dispersal in future studies. We suggest four key improvements: (i) assignment of propagules and/or seedlings; (ii) use of spatial models to inform sampling design; (iii) reducing the influence of unsampled populations and (iv) combined use of nuclear and uniparentally inherited DNA markers to separate gene flow (including pollen and sperm) in general from propagule-mediated dispersal. In combination with direct measurements of seed dispersal these facilitate empirical quantification of dispersal and the detection of uncommon dispersal events, allowing more realistic assessment of spatial population dynamics, relevant for sedentary and relatively immobile organisms.

URL: http://onlinelibrary.wiley.com/doi/10.1111/fwb.12736/pdf

 

Seed dispersal by dabbling ducks: an overlooked dispersal pathway for a broad spectrum of plant species. Soons et al. (2016) Journal of Ecology

Abstract:

  1. Dabbling ducks (Anatinae) are omnivorous birds that are widespread, numerous, highly mobile and often migratory, and therefore have great potential for (long distance) dispersal of other organisms, including plants. However, their ability to act as plant dispersal vectors has received little attention compared to frugivores and is often assumed to be relevant only for wetland species.
  2. To evaluate the potential for plant dispersal by dabbling ducks, we collated and analysed existing data. We identified all plant species whose seeds have been recorded in the diets of the seven dabbling duck (Anas) species in the Western Palaearctic, as reported from gut content analyses. We then analysed the habitats and traits of these plant species to identify general patterns, and related these to data on gut passage survival and duck movements.
  3. A large number of plant species (> 445 species of 189 genera and 57 families) have been recorded in the diet of dabbling ducks. These plant species represent a very wide range of habitats, including almost the full range of site fertility, moisture and light conditions, excluding only very dry and deeply shaded habitats. The ducks prefer seeds of intermediate sizes (1–10 mm3), which have good chances to survive gut passage, but also ingest smaller and larger seeds. Ingested seeds represent a wide range of dispersal syndromes, including fleshy fruits. Many species (62%) were not previously considered animal-dispersed in plant data bases, and 66% were not identified as bird-dispersed. Rarefaction analyses suggest that our analysis still greatly underestimates the total number of plant species ingested.
  4. Synthesis. Dabbling ducks do not exclusively ingest seeds of wetland plants, which make up only 40% of the ingested species. Rather, they feed opportunistically on a wide cross-section of plant species available across the landscapes they inhabit. Given the millions of ducks, the hundreds to thousands of seeds ingested per individual on a daily basis, and known gut passage survival rates, this results in vast numbers of seeds dispersed by ducks per day. Internal seed dispersal by dabbling ducks appears to be a major dispersal pathway for a far broader spectrum of plant species than previously considered.

URL: http://onlinelibrary.wiley.com/doi/10.1111/1365-2745.12531/epdf

 

Summer in the city: behaviour of large gulls visiting an urban area during the breeding season. Huig et al. (2016) Bird Study

Abstract:

Capsule: Large numbers of Herring Gulls Larus argentatus and Lesser Black-backed Gulls Larus fuscus from a traditional colony in the Netherlands visit an urban area for food in the chick rearing period, causing nuisance while doing so.

Aims: To assess the potential contribution of large gulls breeding in a traditional colony to gull–human conflicts in cities.

Methods: Colour-ringed gulls from a nearby colony were counted in the study area throughout the 2014 breeding season. The average numbers observed daily per species and sex were compared between different breeding phases.

Results: Fluctuations in numbers of both species could be explained by breeding phase. Numbers of females of both species and male Lesser Black-backed Gulls dropped significantly during laying and incubation. Numbers peaked post-hatching, coinciding with increased engagement in nuisance events and more frequent displacements within the study area.

Conclusion: Large gulls from a traditional colony frequently visited the urban study area, especially when food demand for chick provisioning was high, suggesting that city visits are motivated by accessibility of urban food. The proportion of rooftop breeding gulls in this area is low. Therefore, measures to avoid nuisance should focus on reducing food availability rather than controlling gull breeding.

URL: http://www.tandfonline.com/doi/pdf/10.1080/00063657.2016.1159179

 

Regurgitation by waterfowl: an overlooked mechanism for long-distance dispersal of wetland plant seeds. Kleyheeg & Van Leeuwen. (2015) Aquatic Botany

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.

URL: http://www.sciencedirect.com/science/article/pii/S030437701530005X

 

Bird-mediated seed dispersal: reduced digestive efficiency in active birds modulates the dispersal capacity of plant seeds. Kleyheeg et al. (2015) Oikos

Abstract: 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 six 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.

URL: http://onlinelibrary.wiley.com/doi/10.1111/oik.01894/full

 

Weak negative associations between avian influenza virus infection and movement behaviour in a key host species, the mallard Anas platyrhynchos. Van Dijk et al. (2015) Oikos

Abstract: Animal movements may contribute to the spread of pathogens. In the case of avian influenza virus, [migratory] birds have been suggested to play a role in the spread of some highly pathogenic strains (e.g. H5N1, H5N8), as well as their low pathogenic precursors which circulate naturally in wild birds. For a better understanding of the emergence and spread of both highly pathogenic (HPAIV) and low pathogenic avian influenza virus (LPAIV), the potential effects of LPAIVs on bird movement need to be evaluated. In a key host species, the mallard Anas platyrhynchos, we tested whether LPAIV infection status affected daily local (< 100 m) and regional (> 100 m) movements by comparing movement behaviour 1) within individuals (captured and sampled at two time points) and 2) between individuals (captured and sampled at one time point). We fitted free-living adult males with GPS loggers throughout the autumn LPAIV infection peak, and sampled them for LPAIV infection at logger deployment and at logger removal on recapture. Within individuals, we found no association between LPAIV infection and daily local and regional movements. Among individuals, daily regional movements of LPAIV infected mallards in the last days of tracking were lower than those of non-infected birds. Moreover, these regional movements of LPAIV infected birds were additionally reduced by poor weather conditions (i.e. increased wind and/or precipitation and lower temperatures). Local movements of LPAIV infected birds in the first days of tracking were higher when temperature decreased. Our study thus demonstrates that bird-assisted dispersal rate of LPAIV may be lower on a regional scale than expected on the basis of the movement behaviour of non-infected birds. Our study underlines the importance of understanding the impact of pathogen infection on host movement in order to assess its potential role in the emergence and spread of infectious diseases.

URL: http://onlinelibrary.wiley.com/doi/10.1111/oik.01836/full

 

Publications in national journals

  • Simons E.L.A.N., Haveman R. & Kleyheeg E. (2016) Revision of Bolboschoenus (Asch.) Palla (Cyperaceae) in the Netherlands. Gorteria, 38:189-223 (pdf)
  • Kleyheeg E. & Oskam C.G.A. (2016) Verrassende prooikeuze van een steenuilenpaar in Zuid-Holland. Limosa, 89:120-123.
  • Huig N., Buijs R.J. & Kleyheeg E. (2016) Foeragerende Zilvermeeuwen langs de Hollandse kust: ‘stadsmeeuwen’ of nog steeds ‘zeemeeuwen’? Limosa, 89:58-66 (pdf)
  • Huig N. & Kleyheeg E. (2015) Partnerruil bij Kleine Mantelmeeuw, uitzondering of regel? Limosa, 88:125-127 (pdf)
  • Kleyheeg E. & Oskam C.G.A. (2015) Geringde Zwarte Stern in Steenuilenkast. Op Het Vinkentouw, 133:31 (pdf)
  • Kleyheeg E. (2013) Beschadigde eendenpoten door aluminium ring. Op Het Vinkentouw, 127:16 (pdf)

 

Publications submitted / under review

  • Poen M.J., Bestebroer T.M., Vuong O., Scheuer R.D., van der Jeugd H.P., Kleyheeg E., Eggink D., Lexmond P., van den Brand J.M.A., Begeman L., van der Vliet S., Müskens G.J.D.M., Majoor F.A., Koopmans M.P.G., Kuiken T. & Fouchier R.A.M. (submitted) Local amplification of highly pathogenic avian influenza H5N8 viruses in wild birds in the Netherlands, 2016-2017.
  • Lameris T.K., Kleyheeg E., Jansen P.A., Brown J. & van Langevelde F. (submited) Nest defendability decreases home range size in central-place foragers.
  • Kleyheeg E., Claessens M. & Soons M.B. (submitted) Interactions between seed traits and digestive processes determine the viability of bird-dispersed seeds.
  • Kleyheeg E., Nolet B., Otero Ojea S. & Soons M.B. (submitted) A mechanistic assessment of the relation between gut morphology and endozoochorous seed dispersal by waterfowl.