Marcel Visser

Prof. dr. Marcel Visser

Afdelingshoofd

Bezoekadres

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands

Over

The Visser-group provided strong empirical evidence that species are responding rapidly to recent anthropogenic climate change. Species shift their seasonal timing (or phenology) but at different rates, which disrupts the temporal synchrony between species

Biografie

Visser is widely recognized as a world-leading expert on the ecological and evolutionary impact of anthropogenic environmental changes. Firstly, he has performed absolute forefront research in understanding how climate change disrupts natural systems, using long-term studies on wild species. His work on phenological mismatch within food chains has turned his model species, the great tit, into the poster child for climate change impact. Visser was the first to use genomic selection to create selection lines for timing of reproduction in a wild vertebrate, and use these to integrate work on epigenetic regulation of gene expression, fitness consequences of timing in the wild, with the impact of climate-change on population numbers.

He is furthermore involved in a wide range of projects, including an Origins Centre project on how to make evolution predictable, bringing together long-term data on populations of individually known birds (SPI-Birds) to make such data FAIR, and more recently he has taken the lead in using data from Long-Term Ecosystem Research sites in the Netherlands (LTER-NL) to create Digital Twins of ecosystems. 

Secondly, he established a unique study on the impact of another anthropogenic environmental change, artificial light at night, on a range of wild taxonomic groups, focussing on how adjusting the colour of night lighting can reduce the negative impact of light at night. He has a world-wide unique, eight times replicated set-up of 20 lampposts in nature and the results of this study have already been implemented in the official guidelines for outdoor illumination. 

Together, these research lines show Visser’s unique strength to bring people together around the crucial next question and sets-up targeted, large-scale experiments that advances the field; working in the wild, under controlled conditions and in the molecular laboratory.

Visser has been awarded a NWO-VICI and an ERC Advanced grant, and has been elected as a member of the Royal Netherlands Academy of Sciences (KNAW). He is co-founder and inaugural president of the Netherlands Society for Evolutionary Biology (NLSEB). Prof Visser has published 225 papers, resulting in an h-index of 62 and >16000 citations making him a Publons Highly Cited Researcher.

Onderzoeksgroepen

CV

Publicaties

Peer-reviewed publicaties

  • Science
    2022

    Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals

    Timothée Bonnet, Michael B. Morrissey, Pierre de Villemereuil, Susan C. Alberts, Peter Arcese, Liam Bailey, Stan Boutin, Patricia Brekke, Lauren J.N. Brent, Glauco Camenisch, Anne Charmantier, Tim H. Clutton-Brock, Andrew Cockburn, David W. Coltman, Alexandre Courtiol, Eve Davidian, Simon R. Evans, John G. Ewen, Marco Festa-Bianchet, Christophe de Franceschi, Lars Gustafsson, Oliver P. Höner, Thomas M. Houslay, Lukas F. Keller, Marta Manser, Andrew G. McAdam, Emily McLean, Pirmin Nietlisbach, Helen L. Osmond, Josephine M. Pemberton, Erik Postma, Jane M. Reid, Alexis Rutschmann, Anna W. Santure, Ben C. Sheldon, Jon Slate, Celine Teplitsky, Marcel E. Visser, Bettina Wachter, Loeske E. B. Kruuk

    The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.

    https://doi.org/10.1126/science.abk0853
  • Molecular Ecology Resources
    2022

    Performance of methods to detect genetic variants from bisulphite sequencing data in a non-model species

    Melanie Lindner, F. Gawehns, Sebastiaan te Molder, Marcel E. Visser, Kees van Oers, Veronika Laine

    The profiling of epigenetic marks like DNA methylation has become a central aspect of studies in evolution and ecology. Bisulphite sequencing is commonly used for assessing genome-wide DNA methylation at single nucleotide resolution but these data can also provide information on genetic variants like single nucleotide polymorphisms (SNPs). However, bisulphite conversion causes unmethylated cytosines to appear as thymines, complicating the alignment and subsequent SNP calling. Several tools have been developed to overcome this challenge, but there is no independent evaluation of such tools for non-model species, which often lack genomic references. Here, we used whole-genome bisulphite sequencing (WGBS) data from four female great tits (Parus major) to evaluate the performance of seven tools for SNP calling from bisulphite sequencing data. We used SNPs from whole-genome resequencing data of the same samples as baseline SNPs to assess common performance metrics like sensitivity, precision, and the number of true positive, false positive, and false negative SNPs for the full range of variant and genotype quality values. We found clear differences between the tools in either optimizing precision (Bis-SNP), sensitivity (biscuit), or a compromise between both (all other tools). Overall, the choice of SNP caller strongly depends on which performance parameter should be maximized and whether ascertainment bias should be minimized to optimize downstream analysis, highlighting the need for studies that assess such differences.

    https://doi.org/10.1111/1755-0998.13493
  • Ecology Letters
    2022

    Temporal correlations among demographic parameters are ubiquitous but highly variable across species

    Rémi Fay, Sandra Hamel, Martijn van de Pol, Jean Michel Gaillard, Nigel G. Yoccoz, Paul Acker, Matthieu Authier, Benjamin Larue, Christie Le Coeur, Kaitlin R. Macdonald, Alex Nicol-Harper, Christophe Barbraud, Christophe Bonenfant, Dirk H. Van Vuren, Emmanuelle Cam, Karine Delord, Marlène Gamelon, Maria Moiron, Fanie Pelletier, Jay J. Rotella, Celine Teplitsky, Marcel E. Visser, Caitlin P. Wells, Nathaniel T. Wheelwright, Stéphanie Jenouvrier, Bernt-Erik Sæther
    Temporal correlations among demographic parameters can strongly influence population dynamics. Our empirical knowledge, however, is very limited regarding the direction and the magnitude of these correlations and how they vary among demographic parameters and species? life histories. Here, we use long-term demographic data from 15 bird and mammal species with contrasting pace of life to quantify correlation patterns among five key demographic parameters: juvenile and adult survival, reproductive probability, reproductive success and productivity. Correlations among demographic parameters were ubiquitous, more frequently positive than negative, but strongly differed across species. Correlations did not markedly change along the slow-fast continuum of life histories, suggesting that they were more strongly driven by ecological than evolutionary factors. As positive temporal demographic correlations decrease the mean of the long-run population growth rate, the common practice of ignoring temporal correlations in population models could lead to the underestimation of extinction risks in most species.
    https://doi.org/10.1111/ele.14026
  • Nature Communications
    2022

    Bird populations most exposed to climate change are less sensitive to climatic variation

    Liam Bailey, Martijn van de Pol, Frank Adriaensen, Aneta Arct, Emilio Barba, Paul E. Bellamy, Suzanne Bonamour, Jean-Charles Bouvier, Malcolm D. Burgess, Anne Charmantier, Camillo A. Cusimano, Blandine Doligez, Szymon M. Drobniak, Anna Dubiec, Marcel Eens, Tapio Eeva, Peter N. Ferns, Anne E. Goodenough, Ian R. Hartley, Shelley A. Hinsley, Elena V. Ivankina, Rimvydas Juškaitis, Bart Kempenaers, Anvar B. Kerimov, Claire Lavigne, Agu Leivits, Mark C. Mainwaring, Erik Matthysen, Jan-Åke Nilsson, Markku Orell, Seppo Rytkönen, Juan Carlos Senar, Ben C. Sheldon, Alberto Sorace, Martyn J. Stenning, János Török, Kees van Oers, Emma Vatka, Stefan Vriend, Marcel E. Visser

    The phenology of many species shows strong sensitivity to climate change; however, with few large scale intra-specific studies it is unclear how such sensitivity varies over a species’ range. We document large intra-specific variation in phenological sensitivity to temperature using laying date information from 67 populations of two co-familial European songbirds, the great tit (Parus major) and blue tit (Cyanistes caeruleus), covering a large part of their breeding range. Populations inhabiting deciduous habitats showed stronger phenological sensitivity than those in evergreen and mixed habitats. However, populations with higher sensitivity tended to have experienced less rapid change in climate over the past decades, such that populations with high phenological sensitivity will not necessarily exhibit the strongest phenological advancement. Our results show that to effectively assess the impact of climate change on phenology across a species’ range it will be necessary to account for intra-specific variation in phenological sensitivity, climate change exposure, and the ecological characteristics of a population.

    https://doi.org/10.1038/s41467-022-29635-4
  • Evolution
    2022

    Population bottleneck has only marginal effect on fitness evolution and its repeatability in dioecious Caenorhabditis elegans

    Karen Bisschop, Thomas Blankers, Janine Mariën, Meike T. Wortel, Martijn Egas, Astrid T. Groot, Marcel E. Visser, Jacintha Ellers

    The predictability of evolution is expected to depend on the relative contribution of deterministic and stochastic processes. This ratio is modulated by effective population size. Smaller effective populations harbor less genetic diversity and stochastic processes are generally expected to play a larger role, leading to less repeatable evolutionary trajectories. Empirical insight into the relationship between effective population size and repeatability is limited and focused mostly on asexual organisms. Here, we tested whether fitness evolution was less repeatable after a population bottleneck in obligately outcrossing populations of Caenorhabditis elegans. Replicated populations founded by 500, 50, or five individuals (no/moderate/strong bottleneck) were exposed to a novel environment with a different bacterial prey. As a proxy for fitness, population size was measured after one week of growth before and after 15 weeks of evolution. Surprisingly, we found no significant differences among treatments in their fitness evolution. Even though the strong bottleneck reduced the relative contribution of selection to fitness variation, this did not translate to a significant reduction in the repeatability of fitness evolution. Thus, although a bottleneck reduced the contribution of deterministic processes, we conclude that the predictability of evolution may not universally depend on effective population size, especially in sexual organisms.

    https://doi.org/10.1111/evo.14556
  • Scientific Reports
    2022

    Integrated molecular and behavioural data reveal deep circadian disruption in response to artificial light at night in male Great tits (Parus major)

    Davide Dominoni, Maaike de Jong, Kees van Oers, Peter O’Shaughnessy, Gavin J. Blackburn, Els Atema, A.C. Mateman, Pietro B. D’Amelio, Lisa Trost, Michelle Bellingham, Jessica Clark, Marcel E. Visser, Barbara Helm

    Globally increasing levels of artificial light at night (ALAN) are associated with shifting rhythms of behaviour in many wild species. However, it is unclear whether changes in behavioural timing are paralleled by consistent shifts in the molecular clock and its associated physiological pathways. Inconsistent shifts between behavioural and molecular rhythms, and between different tissues and physiological systems, disrupt the circadian system, which coordinates all major body functions. We therefore compared behavioural, transcriptional and metabolomic responses of captive great tits (Parus major) to three ALAN intensities or to dark nights, recording activity and sampling brain, liver, spleen and blood at mid-day and midnight. ALAN advanced wake-up time, and this shift was paralleled by advanced expression of the clock gene BMAL1 in all tissues, suggesting close links between behaviour and clock gene expression across tissues. However, further analysis of gene expression and metabolites revealed that clock shifts were inconsistent across physiological systems. Untargeted metabolomic profiling showed that only 9.7% of the 755 analysed metabolites followed the behavioural shift. This high level of desynchronization indicates that ALAN disrupted the circadian system on a deep, easily overlooked level. Thus, circadian disruption could be a key mediator of health impacts of ALAN on wild animals.

    https://doi.org/10.1038/s41598-022-05059-4
  • Frontiers in Ecology and Evolution
    08-12-2021

    11 Pressing Research Questions on How Light Pollution Affects Biodiversity

    Franz Hölker, Janine Bolliger, Thomas W. Davies, Simone Giavi, Andreas Jechow, Gregor Kalinkat, Travis Longcore, Kamiel Spoelstra, Svenja Tidau, Marcel E. Visser, Eva Knop

    Artificial light at night (ALAN) is closely associated with modern societies and is rapidly increasing worldwide. A dynamically growing body of literature shows that ALAN poses a serious threat to all levels of biodiversity—from genes to ecosystems. Many “unknowns” remain to be addressed however, before we fully understand the impact of ALAN on biodiversity and can design effective mitigation measures. Here, we distilled the findings of a workshop on the effects of ALAN on biodiversity at the first World Biodiversity Forum in Davos attended by several major research groups in the field from across the globe. We argue that 11 pressing research questions have to be answered to find ways to reduce the impact of ALAN on biodiversity. The questions address fundamental knowledge gaps, ranging from basic challenges on how to standardize light measurements, through the multi-level impacts on biodiversity, to opportunities and challenges for more sustainable use.

    https://doi.org/10.3389/fevo.2021.767177
  • Journal of Experimental Biology
    01-09-2021

    Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos

    Natalie van Dis, Maurijn van der Zee, Roelof A Hut, Bregje Wertheim, Marcel E. Visser
    Climate change is rapidly altering the environment and many species will need to genetically adapt their seasonal timing to keep up with these changes. Insect development rate is largely influenced by temperature, but we know little about the mechanisms underlying the temperature sensitivity of development. Here, we investigate seasonal timing of egg hatching in the winter moth, one of the few species which has been found to genetically adapt to climate change, likely through selection on temperature sensitivity of egg development rate. To study when during development winter moth embryos are most sensitive to changes in ambient temperature, we gave eggs an increase or decrease in temperature at different moments during their development. We measured their developmental progression and time of egg hatching, and used fluorescence microscopy to construct a timeline of embryonic development for the winter moth. We found that egg development rate responded more strongly to temperature once embryos were in the fully extended germband stage. This is the phylotypic stage at which all insect embryos have developed a rudimentary nervous system. Furthermore, at this stage, timing of ecdysone signaling determines developmental progression, which could act as an environment dependent gateway. Intriguingly, this may suggest that, from the phylotypic stage onward, insect embryos can start to integrate internal and environmental stimuli to actively regulate important developmental processes. As we found evidence that there is genetic variation for temperature sensitivity of egg development rate in our study population, such regulation could be a target of selection imposed by climate change.
    https://doi.org/10.1242/jeb.242554
  • Frontiers in Ecology and Evolution
    22-02-2021

    Integrating Causal and Evolutionary Analysis of Life-History Evolution

    Barbara Tomotani, Phillip Gienapp, Iván De la Hera, Martijn Terpstra, F. Pulido, Marcel E. Visser

    In migratory species, the timing of arrival at the breeding grounds is a life-history trait with major fitness consequences. The optimal arrival date varies from year-to-year, and animals use cues to adjust their arrival dates to match this annual variation. However, which cues they use to time their arrival and whether these cues actually predict the annual optimal arrival date is largely unknown. Here, we integrate causal and evolutionary analysis by identifying the environmental variables used by a migratory songbird to time its arrival dates and testing whether these environmental variables also predicted the optimal time to arrive. We used 11 years of male arrival data of a pied flycatcher population. Specifically, we tested whether temperature and normalized difference vegetation index (NDVI) values from their breeding grounds in the Netherlands and from their wintering grounds in Ivory Coast explained the variation in arrival date, and whether these variables correlated with the position of the annual fitness peak at the breeding grounds. We found that temperature and NDVI, both from the wintering and the breeding grounds, explained the annual variation in arrival date, but did not correlate with the optimal arrival date. We explore three alternative explanations for this lack of correlation. Firstly, the date of the fitness peak may have been incorrectly estimated because a potentially important component of fitness (i.e., migration date dependent mortality en route or directly upon arrival) could not be measured. Secondly, we focused on male timing but the fitness landscape is also likely to be shaped by female timing. Finally, the correlation has recently disappeared because climate change disrupted the predictive value of the cues that the birds use to time their migration. In the latter case, birds may adapt by altering their sensitivity to temperature and NDVI.

    https://doi.org/10.3389/fevo.2021.630823
  • Nature Communications
    2021

    Continent-wide genomic signatures of adaptation to urbanisation in a songbird across Europe

    Pablo Salmón, Arne Jacobs, Dag Ahrén, Clotilde Biard, N.J. Dingemanse, Davide Dominoni, Barbara Helm, Max Lundberg, Juan Carlos Senar, Philipp Sprau, Marcel E. Visser, Caroline Isaksson

    Urbanisation is increasing worldwide, and there is now ample evidence of phenotypic changes in wild organisms in response to this novel environment. Yet, the genetic changes and genomic architecture underlying these adaptations are poorly understood. Here, we genotype 192 great tits (Parus major) from nine European cities, each paired with an adjacent rural site, to address this major knowledge gap in our understanding of wildlife urban adaptation. We find that a combination of polygenic allele frequency shifts and recurrent selective sweeps are associated with the adaptation of great tits to urban environments. While haplotypes under selection are rarely shared across urban populations, selective sweeps occur within the same genes, mostly linked to neural function and development. Collectively, we show that urban adaptation in a widespread songbird occurs through unique and shared selective sweeps in a core-set of behaviour-linked genes.

    https://doi.org/10.1038/s41467-021-23027-w
  • Proceedings of the Royal Society B: Biological Sciences
    2021

    Recent natural variability in global warming weakened phenological mismatch and selection on seasonal timing in great tits (Parus major)

    Marcel E. Visser, Melanie Lindner, Phillip Gienapp, Matthew C. Long, Stephanie Jenouvrier
    Climate change has led to phenological shifts in many species, but with large variation in magnitude among species and trophic levels. The poster child example of the resulting phenological mismatches between the phenology of predators and their prey is the great tit (Parus major), where this mismatch led to directional selection for earlier seasonal breeding. Natural climate variability can obscure the impacts of climate change over certain periods, weakening phenological mismatching and selection. Here, we show that selection on seasonal timing indeed weakened significantly over the past two decades as increases in late spring temperatures have slowed down. Consequently, there has been no further advancement in the date of peak caterpillar food abundance, while great tit phenology has continued to advance, thereby weakening the phenological mismatch. We thus show that the relationships between temperature, phenologies of prey and predator, and selection on predator phenology are robust, also in times of a slowdown of warming. Using projected temperatures from a large ensemble of climate simulations that take natural climate variability into account, we show that prey phenology is again projected to advance faster than great tit phenology in the coming decades, and therefore that long-term global warming will intensify phenological mismatches.
    https://doi.org/10.1098/rspb.2021.1337
  • BMC Genomics
    2021

    Temporal changes in DNA methylation and RNA expression in a small song bird

    Melanie Lindner, Irene C. Verhagen, Heidi M. Viitaniemi, Veronika Laine, Marcel E. Visser, Arild Husby, Kees van Oers

    Background: DNA methylation is likely a key mechanism regulating changes in gene transcription in traits that show temporal fluctuations in response to environmental conditions. To understand the transcriptional role of DNA methylation we need simultaneous within-individual assessment of methylation changes and gene expression changes over time. Within-individual repeated sampling of tissues, which are essential for trait expression is, however, unfeasible (e.g. specific brain regions, liver and ovary for reproductive timing). Here, we explore to what extend between-individual changes in DNA methylation in a tissue accessible for repeated sampling (red blood cells (RBCs)) reflect such patterns in a tissue unavailable for repeated sampling (liver) and how these DNA methylation patterns are associated with gene expression in such inaccessible tissues (hypothalamus, ovary and liver). For this, 18 great tit (Parus major) females were sacrificed at three time points (n = 6 per time point) throughout the pre-laying and egg-laying period and their blood, hypothalamus, ovary and liver were sampled.

    Results: We simultaneously assessed DNA methylation changes (via reduced representation bisulfite sequencing) and changes in gene expression (via RNA-seq and qPCR) over time. In general, we found a positive correlation between changes in CpG site methylation in RBCs and liver across timepoints. For CpG sites in close proximity to the transcription start site, an increase in RBC methylation over time was associated with a decrease in the expression of the associated gene in the ovary. In contrast, no such association with gene expression was found for CpG site methylation within the gene body or the 10 kb up- and downstream regions adjacent to the gene body.

    Conclusion: Temporal changes in DNA methylation are largely tissue-general, indicating that changes in RBC methylation can reflect changes in DNA methylation in other, often less accessible, tissues such as the liver in our case. However, associations between temporal changes in DNA methylation with changes in gene expression are mostly tissue- and genomic location-dependent. The observation that temporal changes in DNA methylation within RBCs can relate to changes in gene expression in less accessible tissues is important for a better understanding of how environmental conditions shape traits that temporally change in expression in wild populations.

    https://doi.org/10.1186/s12864-020-07329-9
  • Journal of Animal Ecology
    2021

    Connecting the data landscape of long-term ecological studies

    Antica Culina, Frank Adriaensen, Liam Bailey, Malcolm D. Burgess, Anne Charmantier, Ella F. Cole, Tapio Eeva, Erik Matthysen, Chloé R. Nater, Ben C. Sheldon, Bernt-Erik Sæther, S.J.G. Vriend, Zuzana Zajkova, Peter Adamík, Lucy M. Aplin, Elena Angulo, Alexandr Artemyev, Emilio Barba, Sanja Barišić, Eduardo Belda, Cemal Can Bilgin, Josefa Bleu, Christiaan Both, Sandra Bouwhuis, Claire J. Branston, Juli Broggi, Terry Burke, Andrey Bushuev, Carlos Camacho, Daniela Campobello, David Canal, Alejandro Cantarero, Samuel P. Caro, Maxime Cauchoix, Alexis Chaine, Mariusz Cichoń, Davor Ćiković, Camillo A. Cusimano, Caroline Deimel, André A Dhondt, N.J. Dingemanse, Blandine Doligez, Davide Dominoni, Claire Doutrelant, Szymon M. Drobniak, Anna Dubiec, Marcel Eens, Kjell Einar Erikstad, Silvia Espín, Damien R. Farine, Jordi Figuerola, Pınar Kavak Gülbeyaz, Arnaud Grégoire, Ian R. Hartley, Michaela Hau, Gergely Hegyi, Sabine Hille, C.A. Hinde, Benedikt Holtmann, Tatyana Ilyina, Caroline Isaksson, Arne Iserbyt, Elena V. Ivankina, Wojciech Kania, Bart Kempenaers, Anvar B. Kerimov, Jan Komdeur, Peter Korsten, Miroslav Král, Miloš Krist, Marcel M. Lambrechts, Carlos E. Lara, Agu Leivits, András Liker, Jaanis Lodjak, Marko Mägi, Mark C. Mainwaring, Raivo Mänd, Bruno Massa, Sylvie Massemin, Jesús Martínez-Padilla, Tomasz D. Mazgajski, Adèle Mennerat, Juan Moreno, Alexia Mouchet, Shinichi Nakagawa, Jan-Åke Nilsson, Johan F. Nilsson, Ana Cláudia Norte, Kees van Oers, Markku Orell, Jaime Potti, John L. Quinn, Denis Réale, Tone Kristin Reiertsen, Balázs Rosivall, Andrew F. Russell, Seppo Rytkönen, Pablo Sánchez-Virosta, Eduardo S.A. Santos, Julia Schroeder, Juan Carlos Senar, Gábor Seress, Tore Slagsvold, Marta Szulkin, Céline Teplitsky, Vallo Tilgar, Andrey Tolstoguzov, János Török, Mihai Valcu, Emma Vatka, Simon Verhulst, Hannah Watson, Teru Yuta, José M. Zamora-Marín, Marcel E. Visser
    The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long‐term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and ecological processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad‐scale global issues (e.g. climate change).
    To solve data integration issues and enable a new scale of ecological and evolutionary research based on long‐term studies of birds, we have created the SPI‐Birds Network and Database (www.spibirds.org)—a large‐scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI‐Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting.
    SPI‐Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collaboration and synthesis. We provide community‐derived data and meta‐data standards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata languages (e.g. ecological meta‐data language).
    The encouraging community involvement stems from SPI‐Bird's decentralized approach: research groups retain full control over data use and their way of data management, while SPI‐Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community‐specific hubs (such as ours, COMADRE for animal demography, etc.) will aid much‐needed large‐scale ecological data integration.
    https://doi.org/10.1111/1365-2656.13388
  • Molecular Ecology
    2021

    Rapid changes in DNA methylation associated with the initiation of reproduction in a small songbird

    Melanie Lindner, Veronika Laine, Irene C. Verhagen, Heidi Viitaniemi, Marcel E. Visser, Kees van Oers, Arild Husby
    Species with a circannual life cycle need to match the timing of their life history events to the environment to maximize fitness. However, our understanding of how circannual traits such as timing of reproduction are regulated on a molecular level remains limited. Recent studies have implicated that epigenetic mechanisms can be an important part in the processes that regulate circannual traits. Here, we explore the role of DNA methylation in mediating reproductive timing in a seasonally breeding bird species, the great tit (Parus major), using genome‐wide DNA methylation data from individual females that were blood sampled repeatedly throughout the breeding season. We demonstrate rapid and directional changes in DNA methylation within the promoter region of several genes, including a key transcription factor (NR5A1) known from earlier studies to be involved in the initiation of timing of reproduction. Interestingly, the observed changes in DNA methylation at NR5A1 identified here are in line with earlier gene expression studies of reproduction in chicken, indicating that the observed shifts in DNA methylation at this gene can have a regulatory role. Our findings provide an important step towards elucidating the genomic mechanism that mediates seasonal timing of a key life history traits and provide support for the idea that epigenetic mechanisms may play an important role in circannual traits.
    https://doi.org/10.1111/mec.15803
  • Journal of Applied Ecology
    2021

    Urban street lighting differentially affects community attributes of airborne and ground-dwelling invertebrate assemblages

    Martin T. Lockett, Therésa M. Jones, Mark A. Elgar, Kevin J. Gaston, Marcel E. Visser, Gareth R. Hopkins

    The introduction of artificial light at night (ALAN) into natural and urbanised landscapes is a known and highly pervasive disruptor of invertebrate communities. However, the effect of variation in intensity and spectra of ALAN on invertebrate communities inhabiting different spatial niches is little understood. Further, the remarkable ability of ALAN to continue to disrupt biodiversity even in chronically illuminated urban landscapes is not often acknowledged. Here, we simultaneously sampled airborne and ground-dwelling invertebrate assemblages under and between urban street lights to explore the effects on community composition and abundance of (a) proximity to decadal (i.e. long-illuminated) nocturnal street lighting and (b) variation in the spectral output of light. The two assemblages responded differently. For airborne invertebrates, night-time abundance doubled, and night-time assemblage composition was significantly different for traps under, compared with between, street lights. These differences in abundance were not affected by street light intensity, and were absent in day samples, suggesting that even weak ALAN may be causing short-term redistribution of nocturnal invertebrates. Further, the abundance (but not composition) effects of ALAN on airborne invertebrates increased when the street lights emitted a higher proportion of short-wavelength light. In contrast, for ground-dwelling invertebrates, we found only marginal effects of proximity and spectrum of lighting on abundance and no effect on assemblage composition. However, more intense street lighting reduced abundance and altered composition at traps both under and between lights. Synthesis and Applications. Public lighting managers must consider ALAN impacts on invertebrate communities not only when introducing ALAN to naïve environments, but also when changing lighting in areas that are highly urbanised and exposed to decades of ALAN. Further, lighting proposals and environmental monitoring of invertebrate communities must take into account the effects on both ground-dwelling and airborne assemblages, as these may respond very differently to the presence, intensity and spectrum of ALAN.

    https://doi.org/10.1111/1365-2664.13969
  • Frontiers in Ecology and Evolution
    2021

    Color of Artificial Light at Night Affects Incubation Behavior in the Great Tit, Parus major

    Artificial light at night (ALAN) has been recognized as a biodiversity threat due to the drastic effects it can have on many organisms. In wild birds, artificial illumination alters many natural behaviors that are important for fitness, including chick provisioning. Although incubation is a key determinant of the early developmental environment, studies into the effects of ALAN on bird incubation behavior are lacking. We measured nest temperature in nest boxes of great tits during the incubation period in two consecutive years. Nest boxes were located in eight previously dark field sites that have been experimentally illuminated since 2012 with white, green, or red light, or were left dark. We tested if light treatment affected mean nest temperature, number of times birds leave the nest (off-bout frequency), and off-bout duration during the incubation period. Subsequently, we investigated if incubation behavior is related to fitness. We found that birds incubating in the white light during a cold, early spring had lower mean nest temperatures at the end of incubation, both during the day and during the night, compared to birds in the green light. Moreover, birds incubating in white light took fewer off-bouts, but off-bouts were on average longer. The opposite was true for birds breeding in the green light. Low incubation temperatures and few but long off-bouts can have severe consequences for developing embryos. In our study, eggs from birds that took on average few off-bouts needed more incubation days to hatch compared to eggs from birds that took many off-bouts. Nevertheless, we found no clear fitness effects of light treatment or incubation behavior on the number of hatchlings or hatchling weight. Our results add to the growing body of literature that shows that effects of ALAN can be subtle, can differ due to the spectral composition of light, and can be year-dependent. These subtle alterations of natural behaviors might not have severe fitness consequences in the short-term. However, in the long term they could add up, negatively affecting parent condition and survival as well as offspring recruitment, especially in urban environments where more environmental pollutants are present.
    https://doi.org/10.3389/fevo.2021.728377
  • Scientific Reports
    27-10-2020

    Pollination and fruit infestation under artificial light at night: light colour matters

    Chiel Boom, Kamiel Spoelstra, Arjen Biere, Eva Knop, Marcel E. Visser
    Rapid human population growth and associated urbanization lead to increased artificial illumination of the environment. By changing the natural light–dark cycle, artificial lighting can affect the functioning of natural ecosystems. Many plants rely on insects in order to reproduce but these insects are known to be disturbed by artificial light. Therefore, plant–insect interactions may be affected when exposed to artificial illumination. These effects can potentially be reduced by using different light spectra than white light. We studied the effect of artificial lighting on plant–insect interactions in the Silene latifolia–Hadena bicruris system using a field set-up with four different light treatments: red, green, white and a dark control. We compared the proportion of fertilized flowers and fertilized ovules as well as the infestation of fruits by Hadena bicruris, a pollinating seed predator. We found no difference in the proportion of fertilized flowers among the treatments. The proportion of fruits infested by H. bicruris was however significantly higher under green and white light and a significantly lower proportion of fertilized ovules was found under green light. We show that artificial light with different colours impacts plant–insect interactions differently, with direct consequences for plant fitness.
    https://doi.org/10.1038/s41598-020-75471-1
  • Current Biology
    22-06-2020

    Experimental light at night has a negative long-term impact on macro-moth populations

    Roy H. A. van Grunsven, Jurriën R. van Deijk, Maurice Donners, Frank Berendse, Marcel E. Visser, Elmar M. Veenendaal, Kamiel Spoelstra
    https://doi.org/10.1016/j.cub.2020.04.083
  • Proceedings of the National Academy of Sciences of the United States of America
    2020

    Fluctuating optimum and temporally variable selection on breeding date in birds and mammals

    Pierre de Villemereuil, Anne Charmantier, Debora Arlt, Pierre Bize, Patricia Brekke, Lyanne Brouwer, Andrew Cockburn, Steeve D Côté, F. Stephen Dobson, Simon Evans, Marco Festa-Bianchet, M. Gamelon, Sandra Hamel, Johann Hegelbach, Kurt Jerstad, Bart Kempenaers, L.E.B. Kruuk, Jouko Kumpula, Thomas Kvalnes, Andrew McAdam, S. Eryn McFarlane, Michael B. Morrissey, Tomas Pärt, Josephine M. Pemberton, Anna Qvarnstrom, Ole W Røstad, Julia Schroeder, Juan Carlos Senar, Ben C. Sheldon, Martijn van de Pol, Marcel E. Visser, Nathaniel T. Wheelwright, Jarle Tufto, Luis-Miguel Chevin
    Temporal variation in natural selection is predicted to strongly impact the evolution and demography of natural populations, with consequences for the rate of adaptation, evolution of plasticity, and extinction risk. Most of the theory underlying these predictions assumes a moving optimum phenotype, with predictions expressed in terms of the temporal variance and autocorrelation of this optimum. However, empirical studies seldom estimate patterns of fluctuations of an optimum phenotype, precluding further progress in connecting theory with observations. To bridge this gap, we assess the evidence for temporal variation in selection on breeding date by modeling a fitness function with a fluctuating optimum, across 39 populations of 21 wild animals, one of the largest compilations of long-term datasets with individual measurements of trait and fitness components. We find compelling evidence for fluctuations in the fitness function, causing temporal variation in the magnitude, but not the direction of selection. However, fluctuations of the optimum phenotype need not directly translate into variation in selection gradients, because their impact can be buffered by partial tracking of the optimum by the mean phenotype. Analyzing individuals that reproduce in consecutive years, we find that plastic changes track movements of the optimum phenotype across years, especially in bird species, reducing temporal variation in directional selection. This suggests that phenological plasticity has evolved to cope with fluctuations in the optimum, despite their currently modest contribution to variation in selection.
    https://doi.org/10.1073/pnas.2009003117
  • Molecular Ecology
    2020

    Host dispersal shapes the population structure of a tick-borne bacterial pathogen

    Ana Claudia Norte, Gabriele Margos, Noemie S. Becker, Jaime Albino Ramos, Maria Sofia Nuncio, Volker Fingerle, Pedro Miguel Araujo, Peter Adamik, Haralambos Alivizatos, Emilio Barba, Rafael Barrientos, Laure Cauchard, Tibor Csorgo, Anastasia Diakou, N.J. Dingemanse, Blandine Doligez, Anna Dubiec, Tapio Eeva, Barbara Flaisz, Tomas Grim, Michaela Hau, Dieter Heylen, Sandor Hornok, Savas Kazantzidis, David Kovats, Frantisek Krause, Ivan Literak, Raivo Mand, Lucia Mentesana, Jennifer Morinay, Marko Mutanen, Julio Manuel Neto, Marketa Novakova, Juan Jose Sanz, Luis Pascoal da Silva, Hein Sprong, Ina-Sabrina Tirri, Janos Torok, Tomi Trilar, Zdenek Tyller, Marcel E. Visser, Isabel Lopes de Carvalho
    Birds are hosts for several zoonotic pathogens. Because of their high mobility, especially of longdistance migrants, birds can disperse these pathogens, affecting their distribution and phylogeography. We focused on Borrelia burgdorferi sensu lato, which includes the causative agents of Lyme borreliosis, as an example for tick‐borne pathogens, to address the role of birds as propagation hosts of zoonotic agents at a large geographical scale. We collected ticks from passerine birds in 11 European countries. B . burgdorferi s.l. prevalence in Ixodes spp. was 37% and increased with latitude. The fieldfare Turdus pilaris and the blackbird T. merula carried ticks with the highest Borrelia prevalence (92 and 58%, respectively), whereas robin Erithacus rubecula ticks were the least infected (3.8%). Borrelia garinii was the most prevalent genospecies (61%), followed by B. valaisiana (24%), B. afzelii (9%), B. turdi (5%) and B. lusitaniae (0.5%). A novel Borrelia genospecies “Candidatus Borrelia aligera” was also detected. Multilocus sequence typing (MLST ) analysis of B. garinii isolates together with the global collection of B. garinii genotypes obtained from the Borrelia MLST public database revealed that: (a) there was little overlap among genotypes from different continents, (b) there was no geographical structuring within Europe, and (c) there was no evident association pattern detectable among B. garinii genotypes from ticks feeding on birds, questing ticks or human isolates. These findings strengthen the hypothesis that the population structure and evolutionary biology of tick‐borne pathogens are shaped by their host associations and the movement patterns of these hosts.
    https://doi.org/10.1111/mec.15336
  • Environmental Pollution
    2020

    Multisensory pollution: Artificial light at night and anthropogenic noise have interactive effects on activity patterns of great tits (Parus major)

    Davide Dominoni, Judith Smit, Marcel E. Visser, Wouter Halfwerk
    Urbanisation is increasing globally at a rapid pace. Consequently, wild species face novel environmental stressors associated with urban sprawl, such as artificial light at night and noise. These stressors have pervasive effects on the behaviour and physiology of many species. Most studies have singled out the impact of just one of these stressors, while in the real world they are likely to co-occur both temporally and spatially, and we thus lack a clear understanding of the combined effect of anthropogenic stressors on wild species. Here, we experimentally exposed captive male great tits (Parus major) to artificial light at night and 24 h noise in a fully factorial experiment. We then measured the effect of both these stressors on their own and their combination on the amount and timing of activity patterns. We found that both light and noise affected activity patterns when presented alone, but in opposite ways: light increased activity, particularly at night, while noise reduced it, particularly during the day. When the two stressors were combined, we found a synergistic effect on the total activity and the nighttime activity, but an antagonistic effect on daytime activity. The significant interaction between noise and light treatment also differed among forest and city birds. Indeed, we detected a significant interactive effect on light and noise on daytime, nighttime, dusktime and offset of activity of urban birds, but not of forest birds. These results suggest that both artificial light at night and anthropogenic noise can drive changes in activity patterns, but that the specific impacts depend on the habitat of origin. Furthermore, our results demonstrate that co-occurring exposure to noise and light can lead to a stronger impact at night than predicted from the additive effects and thus that multisensory pollution may be a considerable threat for wildlife.
    https://doi.org/10.1016/j.envpol.2019.113314
  • Journal of Animal Ecology
    2020

    Comparing two measures of phenological synchrony in a predator–prey interaction: Simpler works better

    Jip Ramakers, Phillip Gienapp, Marcel E. Visser
    Abstract Global climate change has sparked a vast research effort into the demographic and evolutionary consequences of mismatches between consumer and resource phenology. Many studies have used the difference in peak dates to quantify phenological synchrony (match in dates, MD), but this approach has been suggested to be inconclusive, since it does not incorporate the temporal overlap between the phenological distributions (match in overlap, MO). We used 24 years of detailed data on the phenology of a predator?prey system, the great tit (Parus major) and the main food for its nestlings, caterpillars, to estimate MD and MO at the population and brood levels. We compared the performance of both metrics on two key demographic parameters: offspring recruitment probability and selection on the timing of reproduction. Although MD and MO correlated quadratically as expected, MD was a better predictor for both offspring recruitment and selection on timing than MO. We argue?and verify through simulations?that this is because quantifying MO has to be based on nontrivial, difficult-to-verify assumptions that likely render MO too inaccurate as a proxy for food availability in practice. Our results have important implications for the allocation of research efforts in long-term population studies in highly seasonal environments.
    https://doi.org/10.1111/1365-2656.13143
  • Nature Ecology and Evolution
    2020

    International scientists formulate a roadmap for insect conservation and recovery

    Jeff A. Harvey, Robin Heinen, Inge Armbrecht, Yves Basset, James H Baxter-Gilbert, T. Martijn Bezemer, Monika Böhm, Riccardo Bommarco, Paulo A V Borges, Pedro Cardoso, Viola Clausnitzer, Tara Cornelisse, Elizabeth E Crone, Marcel Dicke, Klaas-Douwe B Dijkstra, Lee Dyer, Jacintha Ellers, Thomas Fartmann, Mathew L Forister, Michael J Furlong, Andres Garcia-Aguayo, Justin Gerlach, Rieta Gols, Dave Goulson, Jan-Christian Habel, Nick M Haddad, Caspar A Hallmann, Sérgio Henriques, Marie E Herberstein, Axel Hochkirch, Alice C Hughes, Sarina Jepsen, T Hefin Jones, Bora M Kaydan, David Kleijn, Alexandra-Maria Klein, Tanya Latty, Simon R Leather, Sara M Lewis, Bradford C Lister, John E Losey, Elizabeth C Lowe, Craig R Macadam, James Montoya-Lerma, Christopher D Nagano, Sophie Ogan, Michael C Orr, Christina J Painting, Thai-Hong Pham, Simon G. Potts, Aunu Rauf, Tomas L Roslin, Michael J Samways, Francisco Sanchez-Bayo, Sim A Sar, Cheryl B Schultz, António O Soares, Anchana Thancharoen, Teja Tscharntke, Jason M. Tylianakis, Kate D L Umbers, Louise E.M. Vet, Marcel E. Visser, Ante Vujic, David L Wagner, Michiel F. WallisDeVries, Catrin Westphal, Thomas E White, Vicky L Wilkins, Paul H Williams, Kris A G Wyckhuys, Zeng-Rong Zhu, Hans de Kroon
    https://doi.org/10.1038/s41559-019-1079-8
  • Journal of Evolutionary Biology
    2020

    Quantifying individual variation in reaction norms: Mind the residual

    Jip Ramakers, Marcel E. Visser, Phillip Gienapp
    Abstract Phenotypic plasticity is a central topic in ecology and evolution. Individuals may differ in the degree of plasticity (individual-by-environment interaction (I ? E)), which has implications for the capacity of populations to respond to selection. Random regression models (RRMs) are a popular tool to study I ? E in behavioural or life-history traits, yet evidence for I ? E is mixed, differing between species, populations, and even between studies on the same population. One important source of discrepancies between studies is the treatment of heterogeneity in residual variance (heteroscedasticity). To date, there seems to be no collective awareness among ecologists of its influence on the estimation of I ? E or a consensus on how to best model it. We performed RRMs with differing residual variance structures on simulated data with varying degrees of heteroscedasticity and plasticity, sample size and environmental variability to test how RRMs would perform under each scenario. The residual structure in the RRMs affected the precision of estimates of simulated I ? E as well as statistical power, with substantial lack of precision and high false-positive rates when sample size, environmental variability and plasticity were small. We show that model comparison using information criteria can be used to choose among residual structures and reinforce this point by analysis of real data of two study populations of great tits (Parus major). We provide guidelines that can be used by biologists studying I ? E that, ultimately, should lead to a reduction in bias in the literature concerning the statistical evidence and the reported magnitude of variation in plasticity.
    https://doi.org/10.1111/jeb.13571
  • Ecological Applications
    2020

    Artificial light at night, in interaction with spring temperature, modulates timing of reproduction in a passerine bird

    Davide Dominoni, Johan Kjellberg Jensen, Maaike de Jong, Marcel E. Visser, Kamiel Spoelstra
    Abstract The ecological impact of artificial light at night (ALAN) on phenological events such as reproductive timing is increasingly recognized. In birds, previous experiments under controlled conditions showed that ALAN strongly advances gonadal growth, but effects on egg-laying date are less clear. In particular, effects of ALAN on timing of egg-laying are found to be year-dependent, suggesting an interaction with climatic conditions such as spring temperature, which is known have strong effects on the phenology of avian breeding. Thus, we hypothesized that ALAN and temperature interact to regulate timing of reproduction in wild birds. Field studies have suggested that sources of ALAN rich in short wavelengths can lead to stronger advances in egg-laying date. We therefore tested this hypothesis in the great tit (Parus major), using a replicated experimental setup where eight previously unlit forest transects were illuminated with either white, green, or red LED light, or left dark as controls. We measured timing of egg-laying for 619 breeding events spread over six consecutive years and obtained temperature data for all sites and years. We detected overall significantly earlier egg-laying dates in the white and green light versus the dark treatment, and similar trends for red light. However, there was a strong inter-annual variability in mean egg-laying dates in all treatments, which was explained by spring temperature. We did not detect any fitness consequence of the changed timing of egg-laying due to ALAN, which suggests that advancing reproduction in response to ALAN might be adaptive.
    https://doi.org/10.1002/eap.2062
  • Journal of Experimental Biology
    2020

    Temperature has a causal and plastic effect on timing of breeding in a small songbird

    Irene C. Verhagen, Barbara Tomotani, Phillip Gienapp, Marcel E. Visser
    Phenotypic plasticity is an important mechanism by which an individual can adapt its seasonal timing to predictable, short-term environmental changes by using predictive cues. Identification of these cues is crucial to forecast the response of species to long-term environmental change and to study their potential to adapt. Individual great tits (Parus major) start reproduction early under warmer conditions in the wild, but whether this effect is causal is not well known. We housed 36 pairs of great tits in climate-controlled aviaries and 40 pairs in outdoor aviaries, where they bred under artificial contrasting temperature treatments or in semi-natural conditions, respectively, for two consecutive years, using birds from lines selected for early and late egg laying. We thus obtained laying dates in two different thermal environments for each female. Females bred earlier under warmer conditions in climate-controlled aviaries, but not in outdoor aviaries. The latter was inconsistent with laying dates from our wild population. Further, early selection line females initiated egg laying consistently 9 days earlier than late selection line females in outdoor aviaries, but we found no difference in the degree of plasticity (i.e. the sensitivity to temperature) in laying date between selection lines. Because we found that temperature causally affects laying date, climate change will lead to earlier laying. This advancement is, however, unlikely to be sufficient, thereby leading to selection for earlier laying. Our results suggest that natural selection may lead to a change in mean phenotype, but not to a change in the sensitivity of laying dates to temperature.
    https://doi.org/10.1242/jeb.218784
  • Nature Communications
    2020

    Meta-analysis of multidecadal biodiversity trends in Europe

    Francesca Pilotto, Ingolf Kühn, Rita Adrian, Renate Alber, Audrey Alignier, Christopher Andrews, Jaana Bäck, Luc Barbaro, Deborah Beaumont, Natalie Beenaerts, Sue Benham, David S. Boukal, Vincent Bretagnolle, Elisa Camatti, Roberto Canullo, Patricia G. Cardoso, B.J. Ens, Gert Everaert, Vesela Evtimova, Heidrun Feuchtmayr, Ricardo García-González, Daniel Gómez García, Ulf Grandin, Jerzy M. Gutowski, Liat Hadar, Lubos Halada, Melinda Halassy, Herman Hummel, Kaisa-Leena Huttunen, Bogdan Jaroszewicz, Thomas C. Jensen, Henrik Kalivoda, Inger Kappel Schmidt, Ingrid Kröncke, Reima Leinonen, Filipe Martinho, Henning Meesenburg, Julia Meyer, Stefano Minerbi, Don Monteith, Boris P. Nikolov, Daniel Oro, Dāvis Ozoliņš, Bachisio M. Padedda, Denise Pallett, Marco Pansera, Miguel Ângelo Pardal, Bruno Petriccione, Tanja Pipan, Juha Pöyry, Stefanie M. Schäfer, Marcus Schaub, Susanne C. Schneider, Agnija Skuja, Karline Soetaert, Gunta Spriņģe, Radoslav Stanchev, Jenni A. Stockan, Stefan Stoll, Lisa Sundqvist, Anne Thimonier, Gert Van Hoey, Gunther Van Ryckegem, Marcel E. Visser, Samuel Vorhauser, Peter Haase
    Local biodiversity trends over time are likely to be decoupled from global trends, as local processes may compensate or counteract global change. We analyze 161 long-term biological time series (15–91 years) collected across Europe, using a comprehensive dataset comprising ~6,200 marine, freshwater and terrestrial taxa. We test whether (i) local long-term biodiversity trends are consistent among biogeoregions, realms and taxonomic groups, and (ii) changes in biodiversity correlate with regional climate and local conditions. Our results reveal that local trends of abundance, richness and diversity differ among biogeoregions, realms and taxonomic groups, demonstrating that biodiversity changes at local scale are often complex and cannot be easily generalized. However, we find increases in richness and abundance with increasing temperature and naturalness as well as a clear spatial pattern in changes in community composition (i.e. temporal taxonomic turnover) in most biogeoregions of Northern and Eastern Europe.
    https://doi.org/10.1038/s41467-020-17171-y
  • BMC Genomics
    02-09-2019

    Exploration of tissue-specific gene expression patterns underlying timing of breeding in contrasting temperature environments in a song bird

    Veronika Laine, Irene C. Verhagen, A.C. Mateman, Agata Pijl, Tony D. Williams, Phillip Gienapp, Kees van Oers, Marcel E. Visser
    Seasonal timing of breeding is a life history trait with major fitness consequences but the genetic basis of the physiological mechanism underlying it, and how gene expression is affected by date and temperature, is not well known. In order to study this, we measured patterns of gene expression over different time points in three different tissues of the hypothalamic-pituitary-gonadal-liver axis, and investigated specifically how temperature affects this axis during breeding. We studied female great tits (Parus major) from lines artificially selected for early and late timing of breeding that were housed in two contrasting temperature environments in climate-controlled aviaries. We collected hypothalamus, liver and ovary samples at three different time points (before and after onset of egg-laying). For each tissue, we sequenced whole transcriptomes of 12 pools (n = 3 females) to analyse gene expression.
    https://doi.org/10.1186/s12864-019-6043-0
  • Journal of Experimental Biology
    01-09-2019

    Timing manipulations reveal the lack of a causal link across timing of annual-cycle stages in a long-distance migrant

    Barbara Tomotani, Iván De la Hera, Cynthia Lange, Bart van Lith, Simone L. Meddle, Christiaan Both, Marcel E. Visser
    Organisms need to time their annual-cycle stages, like breeding and migration, to occur at the right time of the year. Climate change has shifted the timing of annual-cycle stages at different rates, thereby tightening or lifting time constraints of these annual-cycle stages, a rarely studied consequence of climate change. The degree to which these constraints are affected by climate change depends on whether consecutive stages are causally linked (scenario I) or whether the timing of each stage is independent of other stages (scenario II). Under scenario I, a change in timing in one stage has knock-on timing effects on subsequent stages, whereas under scenario II, a shift in the timing of one stage affects the degree of overlap with previous and subsequent stages. To test this, we combined field manipulations, captivity measurements and geolocation data. We advanced and delayed hatching dates in pied flycatchers (Ficedula hypoleuca) and measured how the timing of subsequent stages (male moult and migration) were affected. There was no causal effect of manipulated hatching dates on the onset of moult and departure to Africa. Thus, advancing hatching dates reduced the male moult–breeding overlap with no effect on the moult–migration interval. Interestingly, the wintering location of delayed males was more westwards, suggesting that delaying the termination of breeding carries over to winter location. Because we found no causal linkage of the timing of annual-cycle stages, climate change could shift these stages at different rates, with the risk that the time available for some becomes so short that this will have major fitness consequences.
    https://doi.org/10.1242/jeb.201467
  • Methods in Ecology and Evolution
    01-09-2019

    A time-series model for estimating temporal variation in phenotypic selection on laying dates in a Dutch great tit population

    Yihan Cao, Marcel E. Visser, Jarle Tufto
    Abstract Temporal and spatial variation in phenotypic selection due to changing environmental conditions is of great interest to evolutionary biologists, but few existing methods estimating its magnitude take into account the temporal autocorrelation. We use state-space models (SSMs) to analyse phenotypic selection processes that cannot be observed directly and use Template Model builder (TMB), an R package for computing and maximizing the Laplace approximation of the marginal likelihood for SSM and other complex, nonlinear latent variable model via automatic differentiation. Using a long-term great tit (Parus major) dataset, we fit several SSMs and conduct model selection based on Akaike information criterion (AIC) to assess the support for fluctuated directional or autocorrelated stabilizing selection on breeding time of the great tit population. Our results show that there is directional selection on the probability of breeding failure, and stabilizing selection on the mean number of fledglings. This selection for early laying date is consistent with a previous study of the same population. We also estimate the variation and autocorrelation in other parameters of the fitness functions, including the width and height, and found the height and location of annual fitness function are autocorrelated with significant variation, while the width can be assumed to constant over time. Using TMB to fit SSMs, we are able to estimate additional parameters compared to previous methods, all without requiring a substantial increase in computational resources. Furthermore, our specification of complex nonlinear model structure benefits greatly from the flexibility of model formulation with TMB. Therefore, our approach could be directly applied to estimating even more complicated phenotypic selection processes induced by environmental change for other species.
    https://doi.org/10.1111/2041-210X.13249
  • Journal of Experimental Biology
    07-2019

    Short-term, but not long-term, increased daytime workload leads to decreased night-time energetics in a free-living song bird

    Marcel E. Visser, Coby van Dooremalen, Barbara Tomotani, Andrey Bushuev, Harro A. J. Meijer, Luc te Marvelde, Phillip Gienapp
    Reproduction is energetically expensive and to obtain sufficient energy, animals can either alter their metabolic system over time to increase energy intake (increased-intake hypothesis) or reallocate energy from maintenance processes (compensation hypothesis). The first hypothesis predicts a positive relationship between basal metabolic rate (BMR) and energy expenditure (DEE) because of the higher energy demands of the metabolic system at rest. The second hypothesis predicts a trade-off between different body functions, with a reduction of the BMR as a way to compensate for increased daytime energetic expenditure. We experimentally manipulated the workload of wild pied flycatchers by adding or removing chicks when chicks were 2 and 11 days old. We then measured the feeding frequency (FF), DEE and BMR at day 11, allowing us to assess both short- and long-term effects of increased workload. The manipulation at day 2 caused an increase in FF when broods were enlarged, but no response in DEE or BMR, while the manipulation at day 11 caused an increase in FF, no change in DEE and a decrease in BMR in birds with more chicks. Our results suggest that pied flycatchers adjust their workload but that this does not lead to a higher BMR at night (no support for the increased-intake hypothesis). In the short term, we found that birds reallocate energy with a consequent reduction of BMR (evidence for the compensation hypothesis). Birds thus resort to short-term strategies to increase energy expenditure, which could explain why energy expenditure and hard work are not always correlated in birds.
    https://doi.org/10.1242/jeb.199513
  • Evolution Letters
    01-06-2019

    Response to Perrier and Charmantier: On the importance of time scales when studying adaptive evolution

    Mirte Bosse, Lewis G. Spurgin, Veronika Laine, Ella F. Cole, Josh A. Firth, Phillip Gienapp, Andrew G. Gosler, Keith McMahon, Jocelyn Poissant, Irene C. Verhagen, Martien A.M. Groenen, Kees van Oers, Ben C. Sheldon, Marcel E. Visser, Jon Slate
    https://doi.org/10.1002/evl3.112
  • Proceedings of the Royal Society B-Biological Sciences
    15-05-2019

    Personality and gonadal development as sources of individual variation in response to GnRH challenge in female great tits

    Samuel P. Caro, Charlotte A Cornil, Kees van Oers, Marcel E. Visser

    Seasonal timing of reproduction is a key life-history trait, but we know little about the mechanisms underlying individual variation in female endocrine profiles associated with reproduction. In birds, 17β-oestradiol is a key reproductive hormone that links brain neuroendocrine mechanisms, involved in information processing and decision-making, to downstream mechanisms in the liver, where egg-yolk is produced. Here, we test, using a simulated induction of the reproductive system through a Gonadotropin-Releasing Hormone (GnRH) challenge, whether the ovary of pre-breeding female great tits responds to brain stimulation by increasing oestradiol. We also assess how this response is modified by individual-specific traits like age, ovarian follicle size, and personality, using females from lines artificially selected for divergent levels of exploratory behaviour. We show that a GnRH injection leads to a rapid increase in circulating concentrations of oestradiol, but responses varied among individuals. Females with more developed ovarian follicles showed stronger responses and females from lines selected for fast exploratory behaviour showed stronger increases compared to females from the slow line, indicating a heritable component. This study shows that the response of the ovary to reproductive stimulation from the brain greatly varies among individuals and that this variation can be attributed to several commonly measured individual traits, which sheds light on the mechanisms shaping heritable endocrine phenotypes.

    https://doi.org/10.1098/rspb.2019.0142
  • Genome Biology and Evolution
    01-05-2019

    The Genomic Complexity of a Large Inversion in Great Tits

    Vinicius Henrique da Silva, Veronika Laine, Mirte Bosse, Lewis G. Spurgin, Martijn Derks, Kees van Oers, Bert Dibbits, Jon Slate, Richard P.M.A Crooijmans, Marcel E. Visser, Martien A.M. Groenen
    Chromosome inversions have clear effects on genome evolution and have been associated with speciation, adaptation, and the evolution of the sex chromosomes. In birds, these inversions may play an important role in hybridization of species and disassortative mating. We identified a large (\64\ Mb) inversion polymorphism in the great tit (Parus major) that encompasses almost 1,000 genes and more than 90\% of Chromosome 1A. The inversion occurs at a low frequency in a set of over 2,300 genotyped great tits in the Netherlands with only 5\% of the birds being heterozygous for the inversion. In an additional analysis of 29 resequenced birds from across Europe, we found two heterozygotes. The likely inversion breakpoints show considerable genomic complexity, including multiple copy number variable segments. We identified different haplotypes for the inversion, which differ in the degree of recombination in the center of the chromosome. Overall, this remarkable genetic variant is widespread among distinct great tit populations and future studies of the inversion haplotype, including how it affects the fitness of carriers, may help to understand the mechanisms that maintain it.
    https://doi.org/10.1093/gbe/evz106
  • Evolution Letters
    01-04-2019

    Genomic selection on breeding time in a wild bird population

    Phillip Gienapp, Mario P. L. Calus, Veronika Laine, Marcel E. Visser
    Abstract Artificial selection experiments are a powerful tool in evolutionary biology. Selecting individuals based on multimarker genotypes (genomic selection) has several advantages over phenotype-based selection but has, so far, seen very limited use outside animal and plant breeding. Genomic selection depends on the markers tagging the causal loci that underlie the selected trait. Because the number of necessary markers depends, among other factors, on effective population size, genomic selection may be in practice not feasible in wild populations as most wild populations have much higher effective population sizes than domesticated populations. However, the current possibilities of cost-effective high-throughput genotyping could overcome this limitation and thereby make it possible to apply genomic selection also in wild populations. Using a unique dataset of about 2000 wild great tits (Parus major), a small passerine bird, genotyped on a 650 k SNP chip we calculated genomic breeding values for egg-laying date using the so-called GBLUP approach. In this approach, the pedigree-based relatedness matrix of an ?animal model,? a special form of the mixed model, is replaced by a marker-based relatedness matrix. Using the marker-based relatedness matrix, the model seemed better able to disentangle genetic and permanent environmental effects. We calculated the accuracy of genomic breeding values by correlating them to the phenotypes of individuals whose phenotypes were excluded from the analysis when estimating the genomic breeding values. The obtained accuracy was about 0.20, with very little effect of the used genomic relatedness estimator but a strong effect of the number of SNPs. The obtained accuracy is lower than typically seen in domesticated species but considerable for a trait with low heritability (?0.2) as avian breeding time. Our results show that genomic selection is possible also in wild populations with potentially many applications, which we discuss here.
    https://doi.org/10.1002/evl3.103
  • Genome Biology and Evolution
    06-03-2019

    Seasonal Variation in Genome-Wide DNA Methylation Patterns and the Onset of Seasonal Timing of Reproduction in Great Tits

    Heidi Viitaniemi, Irene C. Verhagen, Marcel E. Visser, Antti Honkela, Kees van Oers, Arild Husby
    In seasonal environments, timing of reproduction is a trait with important fitness consequences, but we know little about the molecular mechanisms that underlie the variation in this trait. Recently, several studies put forward DNA methylation as a mechanism regulating seasonal timing of reproduction in both plants and animals. To understand the involvement of DNA methylation in seasonal timing of reproduction, it is necessary to examine within-individual temporal changes in DNA methylation, but such studies are very rare. Here, we use a temporal sampling approach to examine changes in DNA methylation throughout the breeding season in female great tits (Parus major) that were artificially selected for early timing of breeding. These females were housed in climate-controlled aviaries and subjected to two contrasting temperature treatments. Reduced representation bisulfite sequencing on red blood cell derived DNA showed genome-wide temporal changes in more than 40,000 out of the 522,643 CpG sites examined. Although most of these changes were relatively small (mean within-individual change of 6%), the sites that showed a temporal and treatment-specific response in DNA methylation are candidate sites of interest for future studies trying to understand the link between DNA methylation patterns and timing of reproduction.
    https://doi.org/10.1093/gbe/evz044
  • BMC Genomics
    08-01-2019

    Exploring the unmapped DNA and RNA reads in a songbird genome

    Veronika Laine, Toni I Gossmann, Kees van Oers, Marcel E. Visser, Martien A.M. Groenen

    BACKGROUND: A widely used approach in next-generation sequencing projects is the alignment of reads to a reference genome. Despite methodological and hardware improvements which have enhanced the efficiency and accuracy of alignments, a significant percentage of reads frequently remain unmapped. Usually, unmapped reads are discarded from the analysis process, but significant biological information and insights can be uncovered from these data. We explored the unmapped DNA (normal and bisulfite treated) and RNA sequence reads of the great tit (Parus major) reference genome individual. From the unmapped reads we generated de novo assemblies, after which the generated sequence contigs were aligned to the NCBI non-redundant nucleotide database using BLAST, identifying the closest known matching sequence.

    RESULTS: Many of the aligned contigs showed sequence similarity to different bird species and genes that were absent in the great tit reference assembly. Furthermore, there were also contigs that represented known P. major pathogenic species. Most interesting were several species of blood parasites such as Plasmodium and Trypanosoma.

    CONCLUSIONS: Our analyses revealed that meaningful biological information can be found when further exploring unmapped reads. For instance, it is possible to discover sequences that are either absent or misassembled in the reference genome, and sequences that indicate infection or sample contamination. In this study we also propose strategies to aid the capture and interpretation of this information from unmapped reads.

    https://doi.org/10.1186/s12864-018-5378-2
  • Scientific data
    2019

    Temporally replicated reduced representation bisulfate sequencing data on DNA methylation patterns in great tit.

    Hannu Mäkinen, Heidi Viitaniemi, Marcel E. Visser, Irene C. Verhagen, Kees van Oers, Arild Husby
    Seasonal timing of reproduction is an important fitness trait in many plants and animals but the underlying molecular mechanism for this trait is poorly known. DNA methylation is known to affect timing of reproduction in various organisms and is therefore a potential mechanism also in birds. Here we describe genome wide data aiming to detect temporal changes in methylation in relation to timing of breeding using artificial selection lines of great tits (Parus major) exposed to contrasting temperature treatments. Methylation levels of DNA extracted from erythrocytes were examined using reduced representation bisulfite sequencing (RRBS). In total, we obtained sequencing data from 63 libraries over four different time points from 16 birds with on average 20 million quality filtered reads per library. These data describe individual level temporal variation in DNA methylation throughout the breeding season under experimental temperature regimes and provides a resource for future studies investigating the role of temporal changes in DNA methylation in timing of reproduction.
    https://doi.org/10.1038/s41597-019-0136-0
  • Evolution
    2019

    Phenological mismatch drives selection elevation, but not on slope, of breeding time plasticity in a wild songbird

    Jip Ramakers, Phillip Gienapp, Marcel E. Visser
    Phenotypic plasticity is an important mechanism for populations to respond to fluctuating environments, yet may be insufficient to adapt to a directionally changing environment. To study whether plasticity can evolve under current climate change, we quantified selection and genetic variation in both the elevation (RNE) and slope (RNS) of the breeding time reaction norm in a long‐term (1973–2016) study population of great tits (Parus major). The optimal RNE (the caterpillar biomass peak date regressed against the temperature used as cue by great tits) changed over time, whereas the optimal RNS did not. Concordantly, we found strong directional selection on RNE, but not RNS, of egg‐laying date in the second third of the study period; this selection subsequently waned, potentially due to increased between‐year variability in optimal laying dates. We found individual and additive genetic variation in RNE but, contrary to previous studies on our population, not in RNS. The predicted and observed evolutionary change in RNE were, however, marginal, due to low heritability and the sex limitation of laying date. We conclude that adaptation to climate change can only occur via micro‐evolution of RNE, but this will necessarily be slow and potentially hampered by increased variability in phenotypic optima.
    https://doi.org/10.1111/evo.13660
  • Nature Communications
    2019

    Adaptive responses of animals to climate change are most likely insufficient

    Viktoriia Radchuk, Thomas Reed, Céline Teplitsky, Martijn van de Pol, Anne Charmantier, Christopher Hassall, Peter Adamík, Frank Adriaensen, Markus P. Ahola, Peter Arcese, Jesús Miguel Avilés, Javier Balbontin, Karl S. Berg, Antoni Borras, Sarah J. Burthe, Jean Clobert, Nina Dehnhard, Florentino de Lope, André A Dhondt, N.J. Dingemanse, Hideyuki Doi, Tapio Eeva, Joerns Fickel, Iolanda Filella, Frode Fossøy, Anne E. Goodenough, Stephen J. G. Hall, Bengt Hansson, Michael P Harris, Dennis Hasselquist, Thomas Hickler, Jasmin Joshi, Heather Kharouba, Juan Gabriel Martínez, Jean-Baptiste Mihoub, James A Mills, Mercedes Molina-Morales, Arne Moksnes, arpat ozgul, Deseada Parejo, Philippe Pilard, Maud Poisbleau, Francois Rousset, Mark-Oliver Rödel, David Scott, Juan Carlos Senar, Constanti Stefanescu, Bård G. Stokke, Tamotsu Kusano, Maja Tarka, Corey E. Tarwater, Kirsten Thonicke, Jack Thorley, Andreas Wilting, Piotr Tryjanowski, Juha Merilä, Ben C. Sheldon, Anders Pape Møller, Erik Matthysen, Fredric Janzen, F. Stephen Dobson, Marcel E. Visser, Steven R. Beissinger, Alexandre Courtiol, Stephanie Kramer-Schadt
    Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species.
    https://doi.org/10.1038/s41467-019-10924-4
  • Nature Ecology and Evolution
    2019

    Evolutionary and demographic consequences of phenological mismatches

    Marcel E. Visser, Phillip Gienapp
    Climate change has often led to unequal shifts in the seasonal timing (phenology) of interacting species, such as consumers and their resource, leading to phenological ‘mismatches’. Mismatches occur when the time at which a consumer species’s demands for a resource are high does not match with the period when this resource is abundant. Here, we review the evolutionary and population-level consequences of such mismatches and how these depend on other ecological factors, such as additional drivers of selection and density-dependent recruitment. This review puts the research on phenological mismatches into a conceptual framework, applies this framework beyond consumer–resource interactions and illustrates this framework using examples drawn from the vast body of literature on mismatches. Finally, we point out priority questions for research on this key impact of climate change.
    https://doi.org/10.1038/s41559-019-0880-8
  • Functional Ecology
    2019

    Genetic and phenotypic responses to genomic selection for timing of breeding in a wild songbird

    Irene C. Verhagen, Phillip Gienapp, Veronika Laine, Elizabeth van Grevenhof, A.C. Mateman, Kees van Oers, Marcel E. Visser
    The physiological mechanisms underlying avian seasonal timing of reproduction, a life‐history trait with major fitness consequences, are not well understood. Comparing individuals that have been selected to differ in their timing of breeding may prove to be a promising in studying these mechanisms, making selection lines a valuable tool.
    We created selection lines for early and late timing of breeding in great tits (Parus major) using genomic selection, that is selection based on multi‐marker genotypes rather than on the phenotype. We took in nestlings (F1 generation) from wild broods of which the mother was either an extremely early (“early line”) or extremely late (“late line”) breeder. These chicks were then genotyped and, based on their “genomic breeding values” (GEBVs), we selected individuals for early and late line breeding pairs to produce the F2 generation in captivity. The F2 offspring was hand‐reared, genotyped and selected to produce an F3 generation, which were then again genotyped and selected. This way we obtained laying dates in aviaries for F1, F2 and F3 birds.
    We studied the genetic response to the artificial selection and found increased genetic differentiation between the early and late reproducing selection lines over generations (F1–F3), indicated by both diverging GEBVs and increased fixation indices (FST).
    We studied the phenotypic response to selection for birds breeding in outdoor breeding aviaries. We found that early line birds laid earlier than late line birds, and this difference increased over the generations (F1–F3), with non‐significant line effects for the F1 and F2, but highly significant line differences for the F3.
    We also assessed whether there was correlated selection on two traits that are potentially part of the mechanisms underlying seasonal timing: the endogenous free‐running period of the day/night clock (tau) and basal metabolic rate, but found no correlated selection.
    We have successfully created selection lines on seasonal timing in a wild bird species and obtained an instrument for future studies to investigate the physiological mechanisms underlying timing of breeding, and the genetic variation in these mechanisms, an essential component for evolutionary change in timing of reproduction.
    https://doi.org/10.1111/1365-2435.13360
  • American Naturalist
    2019

    Between- and within-individual variation of maternal thyroid hormone deposition in wild great tits (Parus major)

    Bin-Yan Hsu, Irene C. Verhagen, Phillip Gienapp, Veerle M. Darras, Marcel E. Visser, Suvi Ruuskanen
    Maternal hormones are often considered a mediator of anticipatory maternal effects, namely mothers adjust maternal hormone transfer to prepare the offspring for the anticipated environment. The flexibility for mothers to adjust hormone transfer is therefore a prerequisite for such anticipatory maternal effects. Nevertheless, previous studies only focused on the average differences of maternal hormone transfer between groups and neglected the substantial individual variation, despite that individual plasticity on maternal hormone transfer is actually the central assumption. In this study, we studied the between- and within-individual variation of maternal thyroid hormones (THs) in egg yolk of wild great tits (Parus major) and estimated the individual plasticity of maternal yolk THs across environmental temperature, clutch initiation dates and egg laying order using linear mixed-effects models. Interestingly, our models provide statistical evidence that the two main THs – the main biologically active hormone T3, and the prohormone T4 – exhibited different variation patterns. Yolk T3 showed significant between-individual variation on the average levels, in line with its previously reported moderate heritability. Yolk T4, however, showed significant between-clutch variation in the pattern over the laying sequence, suggesting a great within-individual plasticity. Our findings suggest that the role and function of the hormone (pro vs active hormone) within the endocrine axis likely influences its flexibility to respond to environmental change. Whether the flexibility of T4 deposition brings fitness advantage should be examined along with its potential effects on offspring, which remains to be further investigated.
    https://doi.org/10.1086/704738
  • Journal of Experimental Biology
    2019

    Fine-tuning of seasonal timing of breeding is regulated downstream in the underlying neuro-endocrine system in a small songbird

    Irene C. Verhagen, Veronika Laine, A.C. Mateman, Agata Pijl, Ruben de Wit, Bart van Lith, W. Kamphuis, Heidi M. Viitaniemi, Tony D. Williams, Samuel P. Caro, Simone L. Meddle, Phillip Gienapp, Kees van Oers, Marcel E. Visser
    Timing of breeding is under selection in wild populations due to climate change, and understanding the underlying physiological processes mediating timing provides insight in the potential rate of adaptation. Current knowledge on this variation in physiology is, however, mostly limited to males. We assessed whether individual differences in timing of breeding in females are reflected in differences in candidate gene expression and if so, whether these differences occur in the upstream (hypothalamus), or downstream (ovary and liver) parts of the neuroendocrine system. We used 72 female great tits from two generations of lines artificially selected for early and late egg-laying, which were housed in climate controlled aviaries and went through two breeding cycles within one year. In the first breeding season we obtained individual egg-laying dates, while in the second breeding season, using the same individuals, we sampled several tissues at three time points based on timing of the first breeding attempt. For each tissue, mRNA expression levels were measured using qPCR for a set of candidate genes associated with timing of reproduction and subsequently analysed for differences between generations, time points and individual timing of breeding. We found differences in gene expression between generations in all tissues with most pronounced differences in the hypothalamus. Differences between time points, and early and late laying females, were found exclusively in ovary and liver. Altogether, we show that fine-tuning of seasonal timing of breeding, and thereby the opportunity for adaptation in the neuroendocrine system, is regulated mostly downstream in the neuro-endocrine system.
    https://doi.org/10.1242/jeb.202481
  • Current Biology
    2019

    Evolution: Adapting to a Warming World

    Summary To be able to cope with climate change, species need to evolve. Demonstrating such evolution in wild populations is notoriously difficult. Replication of a 21-year-old experiment demonstrates that a long-distance migratory songbird has genetically adapted to climate change.
    https://doi.org/10.1016/j.cub.2019.09.062
  • Frontiers in Ecology and Evolution
    2019

    The Genomics of Circadian Timing in a Wild Bird, the Great Tit (Parus major)

    Veronika Laine, Els Atema, Priscilla Vlaming, Irene C. Verhagen, A.C. Mateman, Jip Ramakers, Kees van Oers, Kamiel Spoelstra, Marcel E. Visser
    Circadian rhythms are ubiquitous among taxa and are essential for coping with recurrent daily events, leading to selection on the properties of the clock underlying these rhythms. To quantify this selection in the wild, we need, however, to phenotype wild individuals, which is difficult using the standard laboratory approach for which individuals need to be kept under constant conditions. To overcome this problem, we explored the possibility to link the variation in a key clock property, circadian period (Tau), to genetic variation. We measured Tau in 152 captive great tits (Parus major). We further linked Tau to two circadian phase markers, the onset of activity in the Light:Dark cycle, and the first onset in constant conditions (Dim:Dim), directly after entrainment. We did a genome-wide association study using a 650k SNP chip, and we linked genetic polymorphisms of a set of twelve candidate genes, to Tau and the two circadian phase markers. In line with earlier studies, Tau was heritable (h2 =0.48 ± 0.22). Despite this genetic variation, we did not find any significant associations at the genome-wide level with the measured traits and only one candidate gene showed association with onset of activity in the Light:Dark cycle. Identifying the genetic base of circadian timing for wild species thus remains challenging. Including alternative molecular methods such as epigenetics or transcriptomics could help to unravel the molecular basis of the biological clock in great tits.
    https://doi.org/10.3389/fevo.2019.00152
  • Journal of Avian Biology
    2019

    Manipulation of photoperiod perception advances gonadal growth but not laying date in the great tit

    Lucia Salis, Samuel P. Caro, Roelof A Hut, Louis Vernooij, Marcel E. Visser
    In seasonal environments, organisms use biotic and abiotic cues to time various biological processes that are crucial for growth, survival and reproductive success. Photoperiod is the best-known cue used to regulate gonadal development, migration and moult of many animal species. In birds, the relationship between photoperiod and gonadal development is clearly established, but we have little understanding on whether photoperiod also regulates actual timing of egg laying under natural conditions. Elucidating the link between photoperiod and timing of breeding is however key to understand whether an evolutionary change in sensitivity to photoperiod is a possible mechanism through which organisms could adjust their seasonal timing in response to climate warming. Here, we investigated the causal relationship between photoperiod, gonadal growth and laying date in wild female great tits. We experimentally increased the photoperiod perceived by the birds in spring by clipping head feathers, and we subsequently monitored gonadal development in the lab and egg laying dates in the wild. We show that our manipulation increased the photoperiod perceived by the birds to a level that approximately corresponds to an advancement of ten calendar days. This increase in perceived photoperiod led to an acceleration of gonadal development, but not to an advancement of egg laying dates. Our results indicate that photoperiod sensitivity is not constraining the advancement of laying date under current environmental conditions and suggest that evolution of sensitivity to other supplementary cues is necessary to advance reproduction under global warming. This article is protected by copyright. All rights reserved.
    https://doi.org/10.1111/jav.02197
  • Proceedings of the Royal Society B-Biological Sciences
    2019

    The preference and costs of sleeping under light at night in forest and urban great tits

    Zeynep Ulgezen, Teemu Käpylä, Peter Meerlo, Kamiel Spoelstra, Marcel E. Visser, Davide Dominoni
    Artificial light at night (ALAN) is an increasing phenomenon associated with worldwide urbanization. In birds, broad-spectrum white ALAN can have disruptive effects on activity patterns, metabolism, stress response and immune function. There has been growing research on whether the use of alternative light spectra can reduce these negative effects, but surprisingly, there has been no study to determine which light spectrum birds prefer. To test such a preference, we gave urban and forest great tits (Parus major) the choice where to roost using pairwise combinations of darkness, white light or green dim light at night (1.5 lux). Birds preferred to sleep under artificial light instead of darkness, and green was preferred over white light. In a subsequent experiment, we investigated the consequence of sleeping under a particular light condition, and measured birds' daily activity levels, daily energy expenditure (DEE), oxalic acid as a biomarker for sleep debt and cognitive abilities. White light affected activity patterns more than green light. Moreover, there was an origin-dependent response to spectral composition: in urban birds, the total daily activity and night activity did not differ between white and green light, while forest birds were more active under white than green light. We also found that individuals who slept under white and green light had higher DEE. However, there were no differences in oxalic acid levels or cognitive abilities between light treatments. Thus, we argue that in naive birds that had never encountered light at night, white light might disrupt circadian rhythms more than green light. However, it is possible that the negative effects of ALAN on sleep and cognition might be observed only under intensities higher than 1.5 lux. These results suggest that reducing the intensity of light pollution as well as tuning the spectrum towards long wavelengths may considerably reduce its impact.
    https://doi.org/10.1098/rspb.2019.0872
  • Ecology and Evolution
    12-2018

    Interspecific transfer of parasites following a range-shift in Ficedula flycatchers

    William Jones, Katarzyna Kulma, Staffan Bensch, Mariusz Cichon, Anvar B. Kerimov, Milos Krist, Toni Laaksonen, Juan Moreno, Pavel Munclinger, Fred M. Slater, Eszter Szollosi, Marcel E. Visser, Anna Qvarnstrom
    Human-induced climate change is expected to cause major biotic changes in species distributions and thereby including escalation of novel host-parasite associations. Closely related host species that come into secondary contact are especially likely to exchange parasites and pathogens. Both the Enemy Release Hypothesis (where invading hosts escape their original parasites) and the Novel Weapon Hypothesis (where invading hosts bring new parasites that have detrimental effects on native hosts) predict that the local host will be most likely to experience a disadvantage. However, few studies evaluate the occurrence of interspecific parasite transfer by performing wide-scale geographic sampling of pathogen lineages, both within and far from host contact zones. In this study, we investigate how haemosporidian (avian malaria) prevalence and lineage diversity vary in two, closely related species of passerine birds; the pied flycatcher Ficedula hypoleuca and the collared flycatcher F. albicollis in both allopatry and sympatry. We find that host species is generally a better predictor of parasite diversity than location, but both prevalence and diversity of parasites vary widely among populations of the same bird species. We also find a limited and unidirectional transfer of parasites from pied flycatchers to collared flycatchers in a recent contact zone. This study therefore rejects both the Enemy Release Hypothesis and the Novel Weapon Hypothesis and highlights the complexity and importance of studying host-parasite relationships in an era of global climate change and species range shifts.
    https://doi.org/10.1002/ece3.4677
  • Frontiers in Ecology and the Environment
    10-2018

    Artificial light at night as a driver of evolution across urban-rural landscapes

    Gareth R. Hopkins, Kevin J. Gaston, Marcel E. Visser, Mark A. Elgar, Theresa M. Jones
    Light is fundamental to biological systems, affecting the daily rhythms of bacteria, plants, and animals. Artificial light at night (ALAN), a ubiquitous feature of urbanization, interferes with these rhythms and has the potential to exert strong selection pressures on organisms living in urban environments. ALAN also fragments landscapes, altering the movement of animals into and out of artificially lit habitats. Although research has documented phenotypic and genetic differentiation between urban and rural organisms, ALAN has rarely been considered as a driver of evolution. We argue that the fundamental importance of light to biological systems, and the capacity for ALAN to influence multiple processes contributing to evolution, makes this an important driver of evolutionary change, one with the potential to explain broad patterns of population differentiation across urban-rural landscapes. Integrating ALAN's evolutionary potential into urban ecology is a targeted and powerful approach to understanding the capacity for life to adapt to an increasingly urbanized world.
    https://doi.org/10.1002/fee.1828
  • PLoS One
    19-09-2018

    Wild great and blue tits do not avoid chemical cues of predators when selecting cavities for roosting

    Luisa Amo de Paz, G. Tomas Gutierrez, Irene Saavedra, Marcel E. Visser
    Small birds use cavities for roosting to decrease the thermoregulatory costs during the winter nights. The ability of birds to detect and escape from an approaching predator is impaired during roosting and thus the selection of such cavities should take into account the risk that a predator will find the cavity. Previous evidence suggested that birds in captivity are able to detect predator scent and avoid roosting in nest-boxes containing such predator chemical cues. Here, we tested whether birds also show this avoidance response under natural conditions. We performed three studies in three populations of blue and great tits. We added predator scent, a pungency scent or an odourless control to nest-boxes and compared the use of these nest-boxes for roosting. We found no differences between the scent treatments in the use of nest-boxes. Therefore, chemical cues indicating the potential presence of a predator are not enough for birds to avoid roosting in nest-boxes under natural conditions.
    https://doi.org/10.1371/journal.pone.0203269
  • Journal of Experimental Zoology Part A: Ecological and Integrative Physiology
    29-07-2018

    Dose-response effects of light at night on the reproductive physiology of great tits (Parus major): Integrating morphological analyses with candidate gene expression

    Davide Dominoni, Maaike de Jong, Michelle Bellingham, Peter O'Shaughnessy, Kees van Oers, Jane Robinson, Bethany Smith, Marcel E. Visser, Barbara Helm
    Abstract Artificial light at night (ALAN) is increasingly recognized as a potential threat to wildlife and ecosystem health. Among the ecological effects of ALAN, changes in reproductive timing are frequently reported, but the mechanisms underlying this relationship are still poorly understood. Here, we experimentally investigated these mechanisms by assessing dose-dependent photoperiodic responses to ALAN in the great tit (Parus major). We individually exposed photosensitive male birds to one of three nocturnal light levels (0.5, 1.5, and 5 lux), or to a dark control. Subsequent histological and molecular analyses on their testes indicated a dose-dependent reproductive response to ALAN. Specifically, different stages of gonadal growth were activated after exposure to different levels of light at night. mRNA transcript levels of genes linked to the development of germ cells (stra8 and spo11) were increased under 0.5 lux compared to the dark control. The 0.5 and 1.5 lux groups showed slight increases in testis size and transcript levels associated with steroid synthesis (lhr and hsd3b1) and spermatogenesis (fshr, wt1, sox9, and cldn11), although spermatogenesis was not detected in histological analysis. In contrast, all birds under 5 lux had 10 to 30 times larger testes than birds in all other groups, with a parallel strong increase in mRNA transcript levels and clear signs of spermatogenesis. Across treatments, the volume of the testes was generally a good predictor of testicular transcript levels. Overall, our findings indicate that even small changes in nocturnal light intensity can increase, or decrease, effects on the reproductive physiology of wild organisms.
    https://doi.org/10.1002/jez.2214
  • Journal of Experimental Zoology Part A: Ecological and Integrative Physiology
    27-06-2018

    Effects of experimental light at night on extra-pair paternity in a songbird

    Maaike de Jong, K.P. Lamers, Mark Eugster, Jenny Ouyang, Arnaud Da Silva, A.C. Mateman, Roy H. A. van Grunsven, Marcel E. Visser, Kamiel Spoelstra
    Abstract Light pollution is increasing worldwide and significantly affects animal behavior. In birds, these effects include advancement of morning activity and onset of dawn song, which may affect extra-pair paternity. Advanced dawn song of males may stimulate females to engage in extra-pair copulations, and the earlier activity onset may affect the males? mate guarding behavior. Earlier work showed an effect of light at night on extra-pair behavior, but this was in an area with other anthropogenic disturbances. Here, we present a two-year experimental study on effects of light at night on extra-pair paternity of great tits (Parus major). Previously dark natural areas were illuminated with white, red, and green LED lamps and compared to a dark control. In 2014, the proportion of extra-pair young in broods increased with distance to the red and white lamps (i.e., at lower light intensities), but decreased with distance to the poles in the dark control. In 2013, we found no effects on the proportion of extra-pair young. The total number of offspring sired by a male was unaffected by artificial light at night in both years, suggesting that potential changes in female fidelity in pairs breeding close to white and red light did not translate into fitness benefits for the males of these pairs. Artificial light at night might disrupt the natural patterns of extra-pair paternity, possibly negates potential benefits of extra-pair copulations and thus could alter sexual selection processes in wild birds.
    https://doi.org/10.1002/jez.2193
  • Global Change Biology
    06-04-2018

    Phenological sensitivity to climate change is higher in resident than in migrant bird populations among European cavity breeders

    Jelmer M. Samplonius, Lenka Bartošová, Malcolm D. Burgess, Andrey Bushuev, Tapio Eeva, Elena V. Ivankina, Anvar B. Kerimov, Indrikis Krams, Toni Laaksonen, Marko Mägi, Raivo Mänd, Jaime Potti, János Török, Miroslav Trnka, Marcel E. Visser, Herwig Zang, Christiaan Both
    Abstract Many organisms adjust their reproductive phenology in response to climate change, but phenological sensitivity to temperature may vary between species. For example, resident and migratory birds have vastly different annual cycles, which can cause differential temperature sensitivity at the breeding grounds, and may affect competitive dynamics. Currently, however, adjustment to climate change in resident and migratory birds have been studied separately or at relatively small geographical scales with varying time series durations and methodologies. Here, we studied differential effects of temperature on resident and migratory birds using the mean egg laying initiation dates from 10 European nest box schemes between 1991 and 2015 that had data on at least one resident tit species and at least one migratory flycatcher species. We found that both tits and flycatchers advanced laying in response to spring warming, but resident tit populations advanced more strongly in relation to temperature increases than migratory flycatchers. These different temperature responses have already led to a divergence in laying dates between tits and flycatchers of on average 0.94 days per decade over the current study period. Interestingly, this divergence was stronger at lower latitudes where the interval between tit and flycatcher phenology is smaller and winter conditions can be considered more favorable for resident birds. This could indicate that phenological adjustment to climate change by flycatchers is increasingly hampered by competition with resident species. Indeed, we found that tit laying date had an additional effect on flycatcher laying date after controlling for temperature, and this effect was strongest in areas with the shortest interval between both species groups. Combined, our results suggest that the differential effect of climate change on species groups with overlapping breeding ecology affects the phenological interval between them, potentially affecting interspecific interactions.
    https://doi.org/10.1111/gcb.14160
  • Proceedings of the Royal Society B-Biological Sciences
    28-03-2018

    Artificial light at night shifts daily activity patterns but not the internal clock in the great tit (Parus major)

    Kamiel Spoelstra, Irene C. Verhagen, Davy Meijer, Marcel E. Visser
    Artificial light at night has shown a dramatic increase over the last decades and continues to increase. Light at night can have strong effects on the behaviour and physiology of species, which includes changes in the daily timing of activity; a clear example is the advance in dawn song onset in songbirds by low levels of light at night. Although such effects are often referred to as changes in circadian timing, i.e. changes to the internal clock, two alternative mechanisms are possible. First, light at night can change the timing of clock controlled activity, without any change to the clock itself; e.g. by a change in the phase relation between the circadian clock and expression of activity. Second, changes in daily activity can be a direct response to light (‘masking’), without any involvement of the circadian system. Here, we studied whether the advance in onset of activity by dim light at night in great tits (Parus major) is indeed attributable to a phase shift of the internal clock. We entrained birds to a normal light/dark (LD) cycle with bright light during daytime and darkness at night, and to a comparable (LDim) schedule with dim light at night. The dim light at night strongly advanced the onset of activity of the birds. After at least six days in LD or LDim, we kept birds in constant darkness (DD) by leaving off all lights so birds would revert to their endogenous, circadian system controlled timing of activity. We found that the timing of onset in DD was not dependent on whether the birds were kept at LD or LDim before the measurement. Thus, the advance of activity under light at night is caused by a direct effect of light rather than a phase shift of the internal clock. This demonstrates that birds are capable of changing their daily activity to low levels of light at night directly, without the need to alter their internal clock.
    https://doi.org/10.1098/rspb.2017.2751
  • American Naturalist
    2018

    Maternal effects in a wild songbird are environmentally plastic but only marginally alter the rate of adaptation

    Jip Ramakers, Marleen Cobben, Piter Bijma, T. E. Reed, Marcel E. Visser, Phillip Gienapp
    Despite ample evidence for the presence of maternal effects (MEs) in a variety of traits and strong theoretical indications for their evolutionary consequences, empirical evidence to what extent MEs can influence evolutionary responses to selection remains ambiguous. We tested the degree to which MEs can alter the rate of adaptation of a key life-history trait, clutch size, using an individual-based model approach parameterized with experimental data from a long-term study of great tits (Parus major). We modeled two types of MEs: (i) an environmentally plastic ME, in which the relationship between maternal and offspring clutch size depended on the maternal environment via offspring condition, and (ii) a fixed ME, in which this relationship was constant. Although both types of ME affected the rate of adaptation following an abrupt environmental shift, the overall effects were small. We conclude that evolutionary consequences of MEs are modest at best in our study system, at least for the trait and the particular type of ME we considered here. A closer link between theoretical and empirical work on MEs would hence be useful to obtain accurate predictions about the evolutionary consequences of MEs more generally.
    https://doi.org/10.1086/696847
  • Journal of Experimental Zoology Part A: Ecological Genetics and Physiology
    2018

    No effect of artificial light of different colors on commuting Daubenton's bats (Myotis daubentonii) in a choice experiment

    Progressive illumination at night poses an increasing threat to species worldwide. Light at night is particularly problematic for bats as most species are nocturnal and often cross relatively large distances when commuting between roosts and foraging grounds. Earlier studies have shown that illumination of linear structures in the landscape disturbs commuting bats, and that the response of bats to light may strongly depend on the light spectrum. Here, we studied the impact of white, green, and red light on commuting Daubenton's bats (Myotis daubentonii). We used a unique location where commuting bats cross a road by flying through two identical, parallel culverts underneath. We illuminated the culverts with white, red, and green light,with an intensity of 5 lux at the water surface. Bats had to choose between the two culverts, each with a different lighting condition every night. We presented all paired combinations of white, green, and red light and dark control in a factorial design. Contrary to our expectations, the number of bat passes through a culvert was unaffected by the presence of light. Furthermore, bats did not show any preference for light color. These results show that the response of commuting Daubenton's bats to different colors of light at night with a realistic intensity may be limited when passing through culverts.
    https://doi.org/10.1002/jez.2178
  • Global Change Biology
    2018

    Climate change leads to differential shifts in the timing of annual cycle stages in a migratory bird

    Barbara Tomotani, Henk P. van der Jeugd, Phillip Gienapp, Iván De la Hera, J. Pilzecker, Corry Teichmann, Marcel E. Visser
    Shifts in reproductive phenology due to climate change have been well documented in many species but how, within the same species, other annual cycle stages (e.g., moult, migration) shift relative to the timing of breeding has rarely been studied. When stages shift at different rates, the interval between stages may change resulting in overlaps, and as each stage is energetically demanding, these overlaps may have negative fitness consequences. We used long-term data of a population of European pied flycatchers (Ficedula hypoleuca) to investigate phenological shifts in three annual cycle stages: spring migration (arrival dates), breeding (egg-laying and hatching dates) and the onset of post-breeding moult. We found different advancements in the timing of breeding compared to moult (moult advances faster) and no advancement in arrival dates. To understand these differential shifts, we explored which temperatures best explain the year-to-year variation in the timing of these stages, and show that they respond differently to temperature increases in the Netherlands, causing the intervals between arrival and breeding and between breeding and moult to decrease. Next, we tested the fitness consequences of these shortened intervals. We found no effect on clutch size, but the probability of a fledged chick to recruit increased with a shorter arrival-breeding interval (earlier breeding). Finally, mark-recapture analyses did not detect an effect of shortened intervals on adult survival. Our results suggest that the advancement of breeding allows more time for fledgling development, increasing their probability to recruit. This may incur costs to other parts of the annual cycle but, despite the shorter intervals, there was no effect on adult survival. Our results show that to fully understand the consequences of climate change, it is necessary to look carefully at different annual cycle stages, especially for organisms with complex cycles, such as migratory birds.
    https://doi.org/10.1111/gcb.14006
  • BMC Genomics
    2018

    CNVs are associated with genomic architecture in a songbird

    Vinicius Henrique da Silva, Veronika Laine, Mirte Bosse, Kees van Oers, B.W. Dibbits, Marcel E. Visser, Richard P. M. A. Crooijmans, Martien A.M. Groenen
    Understanding variation in genome structure is essential to understand phenotypic differences within populations and the evolutionary history of species. A promising form of this structural variation is copy number variation (CNV). CNVs can be generated by different recombination mechanisms, such as non-allelic homologous recombination, that rely on specific characteristics of the genome architecture. These structural variants can therefore be more abundant at particular genes ultimately leading to variation in phenotypes under selection. Detailed characterization of CNVs therefore can reveal evolutionary footprints of selection and provide insight in their contribution to phenotypic variation in wild populations.
    https://doi.org/10.1186/s12864-018-4577-1
  • Nature Ecology and Evolution
    2018

    Navigating the unfolding open data landscape in ecology and evolution

    Antica Culina, Miriam Baglioni, Tom Crowther, Marcel E. Visser, Saskia Woutersen, P. Manghi
    Open access to data is revolutionizing the sciences. To allow ecologists and evolutionary biologists to confidently find and use the existing data, we provide an overview of the landscape of online data infrastructures, and highlight the key points to consider when using open data. We introduce an online collaborative platform to keep a community-driven, updated list of the best sources that enable search for data in one interface. In doing so, our aim is to lower the barrier to accessing open data, and encourage its use by researchers hoping to increase the scope, reliability and value of their findings.
    https://doi.org/10.1038/s41559-017-0458-2
  • New Phytologist
    2018

    Covariation and phenotypic integration in chemical communication displays: biosynthetic constraints and eco-evolutionary implications

    Robert R. Junker, Jonas Kuppler, Luisa Amo de Paz, James D. Blande, Renee M. Borges, Nicole M. van Dam, Marcel Dicke, Stefan Dötterl, Bodil K. Ehlers, Florian Etl, Jonathan Gershenzon, Robert Glinwood, Rieta Gols, Astrid T. Groot, Martin Heil, Mathias Hoffmeister, Jarmo K. Holopainen, Stefan Jarau, Lena John, André Kessler, Jette T. Knudsen, Christian Kost, Anne-Amélie C. Larue-Kontic, Sara Diana Leonhardt, Dani Lucas-Barbosa, Cassie J. Majetic, Florian Menzel, Amy L. Parachnowitsch, Rémy S. Pasquet, Erik H. Poelman, Robert A. Raguso, Joachim Ruther, FLORIAN P. SCHIESTL, Thomas Schmitt, Dorothea Tholl, Sybille B. Unsicker, Niels Verhulst, Marcel E. Visser, Berhane T. Weldegergis, Tobias G. Köllner
    •Chemical communication is ubiquitous. The identification of conserved structural elements in visual and acoustic communication is well established, but comparable information on chemical communication displays (CCDs) is lacking.
    •We assessed the phenotypic integration of CCDs in a meta-analysis to characterize patterns of covariation in CCDs and identified functional or biosynthetically constrained modules.
    •Poorly integrated plant CCDs (i.e. low covariation between scent compounds) support the notion that plants often utilize one or few key compounds to repel antagonists or to attract pollinators and enemies of herbivores. Animal CCDs (mostly insect pheromones) were usually more integrated than those of plants (i.e. stronger covariation), suggesting that animals communicate via fixed proportions among compounds. Both plant and animal CCDs were composed of modules, which are groups of strongly covarying compounds. Biosynthetic similarity of compounds revealed biosynthetic constraints in the covariation patterns of plant CCDs.
    •We provide a novel perspective on chemical communication and a basis for future investigations on structural properties of CCDs. This will facilitate identifying modules and biosynthetic constraints that may affect the outcome of selection and thus provide a predictive framework for evolutionary trajectories of CCDs in plants and animals.
    https://doi.org/10.1111/nph.14505
  • Functional Ecology
    2018

    Photoperiodic cues regulate phenological carry-over effects in an herbivorous insect

    Lucia Salis, E. van den Hoorn, Domien G. M. Beersma, Roelof A Hut, Marcel E. Visser
    To maximise their fitness, organisms need to synchronise their phenology with the seasonal variation in environmental conditions. Most phenological traits are affected by environmental abiotic cues such as photoperiod, temperature and rainfall. When individuals with complex life cycles fail to match one of the stages with the favourable environment, the negative conditions experienced may lead to carry-over effects and, thus, influence fitness in subsequent stages.
    In the winter moth, an herbivorous insect with an annual life cycle, timing of egg-hatching in spring is strongly influenced by temperature and varies from year to year. To investigate whether the phenological variation in egg-hatching date affects subsequent stages, we analysed data on egg-hatching date and adult catching date (considered here to be a proxy for adult eclosion date) from our long-term study (1994–2014). Furthermore, we experimentally manipulated the photoperiod experienced by newly hatched larvae and recorded the phenology of their subsequent life cycle stages.
    In the long-term field study, we found that the timing of winter moth egg-hatching in spring varied strongly from year to year. Interestingly, however, the timing of adult eclosion date in winter showed little inter-annual variation. In line with these findings, our experimental data showed that the winter moth shortened the duration of their pupal development when they experienced a late spring photoperiod as a larva, and prolonged pupal development when experiencing early spring photoperiod. The effects of the larval photoperiodic treatments persisted during egg development in the following generation.
    The results show that a phenological shift that occurs during an early life stage is partially compensated during subsequent stages and suggest that the mechanism underlying this compensation is mediated by photoperiod. Winter moths regulated their phenology in such a way that the variation in the egg-hatching stage was not carried over to the next life cycle stages. This has strong effects on fitness as it (1) ensures the synchronisation of adult eclosion during the mating period and (2) is likely to reduce potentially negative fitness consequences of phenological mismatches in egg-hatching in the following generation. Overall, these findings stress the importance of understanding phenological carry-over effects to forecast the impact of global change in species with complex life cycles.
    https://doi.org/10.1111/1365-2435.12953
  • Nature Ecology and Evolution
    2018

    How to do meta-analysis of open datasets

    Antica Culina, Tom Crowther, Jip Ramakers, Phillip Gienapp, Marcel E. Visser
    The amount of open data in ecology and evolution is increasing rapidly, yet this resource remains underused. Here, we introduce a new framework and case study for conducting meta-analyses of open datasets, and discuss its benefits and current limitations.
    https://doi.org/10.1038/s41559-018-0579-2
  • Molecular Ecology Resources
    2018

    A high density SNP chip for genotyping great tit (Parus major) populations and its application to studying the genetic architecture of exploration behaviour

    Jung-Mi Kim, A.W. Santure, Henry J Barton, J.L. Quinn, Eleanor F. Cole, Marcel E. Visser, Ben C. Sheldon, M.A.M. Groenen, Kees van Oers, Jon Slate
    High density SNP microarrays (‘SNP chips’) are a rapid, accurate and efficient method for genotyping several hundred thousand polymorphisms in large numbers of individuals. While SNP chips are routinely used in human genetics and in animal and plant breeding, they are less widely used in evolutionary and ecological research. In this paper we describe the development and application of a high density Affymetrix Axiom chip with around 500 000 SNPs, designed to perform genomics studies of great tit (Parus major) populations. We demonstrate that the per‐SNP genotype error rate is well below 1% and that the chip can also be used to identify structural or copy number variation (CNVs). The chip is used to explore the genetic architecture of exploration behaviour (EB), a personality trait that has been widely studied in great tits and other species. No SNPs reached genome‐wide significance, including at DRD4, a candidate gene. However, EB is heritable and appears to have a polygenic architecture. Researchers developing similar SNP chips may note: (i) SNPs previously typed on alternative platforms are more likely to be converted to working assays, (ii) detecting SNPs by more than one pipeline, and in independent datasets, ensures a high proportion of working assays, (iii) allele frequency ascertainment bias is minimised by performing SNP discovery in individuals from multiple populations and (iv) samples with the lowest call rates tend to also have the greatest genotyping error rates.
    https://doi.org/10.1111/1755-0998.12778
  • Nature Ecology and Evolution
    2018

    Environmental coupling of heritability and selection is rare and of minor evolutionary significance in wild populations

    Jip Ramakers, Antica Culina, Marcel E. Visser, Phillip Gienapp
    Predicting the rate of adaptation to environmental change in wild populations is important for understanding evolutionary
    change. However, predictions may be unreliable if the two key variables affecting the rate of evolutionary change—heritability
    and selection—are both affected by the same environmental variable. To determine how general such an environmentally
    induced coupling of heritability and selection is, and how this may influence the rate of adaptation, we made use of freely accessible,
    open data on pedigreed wild populations to answer this question at the broadest possible scale. Using 16 populations from 10 vertebrate species, which provided data on 50 traits (relating to body mass, morphology, physiology, behaviour and
    life history), we found evidence for an environmentally induced relationship between heritability and selection in only 6 cases, with weak evidence that this resulted in an increase or decrease in the expected selection response. We conclude that such a coupling of heritability and selection is unlikely to strongly affect evolutionary change, even though both heritability and selection are commonly postulated to be dependent on the environment.
    https://doi.org/10.1038/s41559-018-0577-4
  • Functional Ecology
    2018

    Simulated moult reduces flight performance but overlap with breeding does not affect breeding success in a long-distance migrant

    Barbara Tomotani, Florian T. Muijres, Julia Koelman, Stefania Casagrande, Marcel E. Visser
    * Long-distance migrants are time-constrained as they need to incorporate many annual cycle stages within a year. Migratory passerines moult in the short interval between breeding and migration. To widen this interval, moult may start while still breeding, but this results in flying with moulting wings when food provisioning. * We experimentally simulated wing gaps in breeding male pied flycatchers by plucking two primary feathers from both wings. We quantified the nest visitations of both parents, proportion of high-quality food brought to the nestlings and adults and nestlings condition. Differences in oxidative damage caused by a possible reduction in flight efficiency were measured in amounts of ROMs and OXY in the blood. We also measured how flight performance was affected with recordings of the male`s escape flight using high-speed cameras. Finally, we collected data on adult survival, clutch size and laying date in the following year. * “Plucked” males travelled a 5% shorter distance per wingbeat, showing that our treatment reduced flight performance. In line with this, “plucked” males visited their nests less often. Females of “plucked” males, however, visited the nest more often than controls, and fully compensated their partner's reduced visitation rate. As a result, there were no differences between treatments in food quality brought to the nest, adult or chick mass or number of successfully fledged chicks. Males did not differ in their oxidative damage or local survival to the following year. In contrast, females paired with plucked males tended to return less often to breed in the next year in comparison to controls, but this difference was not significant. For the birds that did return, there were no effects on breeding. * Our results reveal that wing gaps in male pied flycatchers reduce their flight performance, but when it occurs during breeding they prioritise their future reproduction by reducing parental care. As a result, there is no apparent detriment to their condition during breeding. Because non-moulting females are able to compensate their partner's reduced care, there is also no immediate cost to the offspring, but females may pay the cost suffering from a reduced survival. A plain language summary is available for this article.
    https://doi.org/10.1111/1365-2435.12974
  • Ardea
    2018

    Timing of avian breeding in an urbanized world

    Maaike de Jong, L. Van den Eertwegh, R. Beskers, Peter De Vries, Kamiel Spoelstra, Marcel E. Visser
    A large part of the world is urbanized, and the process of urbanization is ongoing.
    Species differ in the extent to which they are impacted by urbanization, depending
    on adaption capacity, and on the fitness consequences when adaptation lags
    behind. One prominent effect of urbanization is the dramatic change of the nighttime
    environment: in urban areas nights are no longer dark. Here, we studied the
    impact of urbanization on the timing of breeding, which is a key life-history trait.
    We used six years of data from ten common bird species, breeding in nest boxes
    throughout the Netherlands. We took the intensity of artificial light in the form of
    zenithal sky brightness and light emission, as a proxy for urbanization. We found
    a correlation between light levels and seasonal timing in three of the ten species
    (great tit, blue tit and pied flycatcher), but these relationships differed between
    years. The effect of urbanization on seasonal timing is at best weak in our study
    which was however mainly based on areas with relatively low light levels. There is
    a clear lack of data for breeding birds in more urbanized environments, an ever
    expanding habitat for an increasing number of species worldwide.
    https://doi.org/10.5253/arde.v106i1.a4
  • Genome Biology and Evolution
    01-11-2017

    Determinants of the Efficacy of Natural Selection on Coding and Noncoding Variability in Two Passerine Species

    Pádraic Corcoran, Toni I Gossmann, Henry J Barton, Jon Slate, Kai Zeng, Veronika Laine, Kees van Oers, Koen Verhoeven, Marcel E. Visser
    Population genetic theory predicts that selection should be more effective when the effective population size (Ne) is larger, and that the efficacy of selection should correlate positively with recombination rate. Here, we analyzed the genomes of ten great tits and ten zebra finches. Nucleotide diversity at 4-fold degenerate sites indicates that zebra finches have a 2.83-fold larger Ne. We obtained clear evidence that purifying selection is more effective in zebra finches. The proportion of substitutions at 0-fold degenerate sites fixed by positive selection (α) is high in both species (great tit 48%; zebra finch 64%) and is significantly higher in zebra finches. When α was estimated on GC-conservative changes (i.e., between A and T and between G and C), the estimates reduced in both species (great tit 22%; zebra finch 53%). A theoretical model presented herein suggests that failing to control for the effects of GC-biased gene conversion (gBGC) is potentially a contributor to the overestimation of α, and that this effect cannot be alleviated by first fitting a demographic model to neutral variants. We present the first estimates in birds for α in the untranslated regions, and found evidence for substantial adaptive changes. Finally, although purifying selection is stronger in high-recombination regions, we obtained mixed evidence for α increasing with recombination rate, especially after accounting for gBGC. These results highlight that it is important to consider the potential confounding effects of gBGC when quantifying selection and that our understanding of what determines the efficacy of selection is incomplete.
    https://doi.org/10.1093/gbe/evx213
  • Science
    20-10-2017

    Recent natural selection causes adaptive evolution of an avian polygenic trait

    Mirte Bosse, Lewis G. Spurgin, Veronika Laine, Ella F. Cole, Josh A. Firth, Phillip Gienapp, Andrew G. Gosler, Keith McMahon, Jocelyn Poissant, Irene C. Verhagen, Martien A.M. Groenen, Kees van Oers, Ben C. Sheldon, Marcel E. Visser, Jon Slate
    Many studies have found evidence of rapid evolution in response to environmental change. In most cases, there has been some suggestion of which traits might be most responsive ahead of time. Bosse et al. turn this approach on its head by using genomic regions with a signature of selection to identify traits that are changing. In great tits (Parus major) in the United Kingdom, genomic regions showing selection invariably contained genes associated with bill growth. Indeed, U.K. birds not only have longer bills, but these longer bills are associated with increased fitness. These changes likely reflect an increase in domestic garden bird feeders over the past several decades.Science, this issue p. 365We used extensive data from a long-term study of great tits (Parus major) in the United Kingdom and Netherlands to better understand how genetic signatures of selection translate into variation in fitness and phenotypes. We found that genomic regions under differential selection contained candidate genes for bill morphology and used genetic architecture analyses to confirm that these genes, especially the collagen gene COL4A5, explained variation in bill length. COL4A5 variation was associated with reproductive success, which, combined with spatiotemporal patterns of bill length, suggested ongoing selection for longer bills in the United Kingdom. Last, bill length and COL4A5 variation were associated with usage of feeders, suggesting that longer bills may have evolved in the United Kingdom as a response to supplementary feeding.
    https://doi.org/10.1126/science.aal3298
  • Integrative and Comparative Biology
    16-10-2017

    Understanding Evolutionary Impacts of Seasonality: An Introduction to the Symposium

    Caroline M. Williams, Gregory J. Ragland, Gustavo Betini, Lauren B. Buckley, Zachary A. Cheviron, Kathleen Donohue, Joe Hereford, Murray M. Humphries, Simeon Lisovski, Katie E. Marshall, Paul S. Schmidt, Kimberly S. Sheldon, Øystein Varpe, Marcel E. Visser
    Seasonality is a critically important aspect of environmental variability, and strongly shapes all aspects of life for organisms living in highly seasonal environments. Seasonality has played a key role in generating biodiversity, and has driven the evolution of extreme physiological adaptations and behaviors such as migration and hibernation. Fluctuating selection pressures on survival and fecundity between summer and winter provide a complex selective landscape, which can be met by a combination of three outcomes of adaptive evolution: genetic polymorphism, phenotypic plasticity, and bet-hedging. Here, we have identified four important research questions with the goal of advancing our understanding of evolutionary impacts of seasonality. First, we ask how characteristics of environments and species will determine which adaptive response occurs. Relevant characteristics include costs and limits of plasticity, predictability, and reliability of cues, and grain of environmental variation relative to generation time. A second important question is how phenological shifts will amplify or ameliorate selection on physiological hardiness. Shifts in phenology can preserve the thermal niche despite shifts in climate, but may fail to completely conserve the niche or may even expose life stages to conditions that cause mortality. Considering distinct environmental sensitivities of life history stages will be key to refining models that forecast susceptibility to climate change. Third, we must identify critical physiological phenotypes that underlie seasonal adaptation and work toward understanding the genetic architectures of these responses. These architectures are key for predicting evolutionary responses. Pleiotropic genes that regulate multiple responses to changing seasons may facilitate coordination among functionally related traits, or conversely may constrain the expression of optimal phenotypes. Finally, we must advance our understanding of how changes in seasonal fluctuations are impacting ecological interaction networks. We should move beyond simple dyadic interactions, such as predator prey dynamics, and understand how these interactions scale up to affect ecological interaction networks. As global climate change alters many aspects of seasonal variability, including extreme events and changes in mean conditions, organisms must respond appropriately or go extinct. The outcome of adaptation to seasonality will determine responses to climate change.
    https://doi.org/10.1093/icb/icx122
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    09-10-2017

    Chronobiology of interspecific interactions in a changing world

    Noga Kronfeld-Schor, Marcel E. Visser, Lucia Salis, J.A. Van Gils
    Animals should time activities, such as foraging, migration and reproduction, as well as seasonal physiological adaptation, in a way that maximizes fitness. The fitness outcome of such activities depends largely on their interspecific interactions; the temporal overlap with other species determines when they should be active in order to maximize their encounters with food and to minimize their encounters with predators, competitors and parasites. To cope with the constantly changing, but predictable structure of the environment, organisms have evolved internal biological clocks, which are synchronized mainly by light, the most predictable and reliable environmental cue (but which can be masked by other variables), which enable them to anticipate and prepare for predicted changes in the timing of the species they interact with, on top of responding to them directly. Here, we review examples where the internal timing system is used to predict interspecific interactions, and how these interactions affect the internal timing system and activity patterns. We then ask how plastic these mechanisms are, how this plasticity differs between and within species and how this variability in plasticity affects interspecific interactions in a changing world, in which light, the major synchronizer of the biological clock, is no longer a reliable cue owing to the rapidly changing climate, the use of artificial light and urbanization.This article is part of the themed issue ‘Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals’.
    https://doi.org/10.1098/rstb.2016.0248
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    09-10-2017

    Two sides of a coin: ecological and chronobiological perspectives of timing in the wild

    Barbara Helm, Marcel E. Visser, William Schwartz, Noga Kronfeld-Schor, Menno Gerkema, Theunis Piersma, Guy Bloch
    Most processes within organisms, and most interactions between organisms and their environment, have distinct time profiles. The temporal coordination of such processes is crucial across levels of biological organization, but disciplines differ widely in their approaches to study timing. Such differences are accentuated between ecologists, who are centrally concerned with a holistic view of an organism in relation to its external environment, and chronobiologists, who emphasize internal timekeeping within an organism and the mechanisms of its adjustment to the environment. We argue that ecological and chronobiological perspectives are complementary, and that studies at the intersection will enable both fields to jointly overcome obstacles that currently hinder progress. However, to achieve this integration, we first have to cross some conceptual barriers, clarifying prohibitively inaccessible terminologies. We critically assess main assumptions and concepts in either field, as well as their common interests. Both approaches intersect in their need to understand the extent and regulation of temporal plasticity, and in the concept of ‘chronotype’, i.e. the characteristic temporal properties of individuals which are the targets of natural and sexual selection. We then highlight promising developments, point out open questions, acknowledge difficulties and propose directions for further integration of ecological and chronobiological perspectives through Wild Clock research.This article is part of the themed issue ‘Wild Clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals’.
    https://doi.org/10.1098/rstb.2016.0246
  • Journal of Biological Rhythms
    26-07-2017

    Early Birds by Light at Night: Effects of Light Color and Intensity on Daily Activity Patterns in Blue Tits

    Maaike de Jong, Samuel P. Caro, Phillip Gienapp, Kamiel Spoelstra, Marcel E. Visser
    Artificial light at night disturbs the daily rhythms of many organisms. To what extent this disturbance depends on the intensity and spectral composition of light remain obscure. Here, we measured daily activity patterns of captive blue tits (Cyanistes caeruleus) exposed to similar intensities of green, red, or white light at night. Birds advanced their onset of activity in the morning under all light colors but more under red and white light than under green light. Offset of activity was slightly delayed in all light colors. The total activity over a 24-h period did not change but birds moved a part of their daily activity into the night. Since the effect of red and white lights are comparable, we tested the influence of light intensity in a follow-up experiment, where we compared the activity of the birds under different intensities of green and white light only. While in the higher range of intensities, the effects of white and green light were comparable; at lower intensities, green light had a less disturbing effect as compared with white light on daily rhythms in blue tits. Our results show that the extent of this disturbance can be mitigated by modulating the spectral characteristics and intensity of outdoor lighting, which is now feasible through the use of LED lighting.
    https://doi.org/10.1177/0748730417719168
  • Proceedings of the Royal Society B-Biological Sciences
    06-2017

    Response of bats to light with different spectra: light-shy and agile bat presence is affected by white and green, but not red light

    Kamiel Spoelstra, Roy H. A. van Grunsven, Jip Ramakers, Kim Ferguson, Thomas Raap, Maurice Donners, Elmar M. Veenendaal, Marcel E. Visser
    Artificial light at night has shown a remarkable increase over the past decades. Effects are reported for many species groups, and include changes in presence, behaviour, physiology and life-history traits. Among these, bats are strongly affected, and how bat species react to light is likely to vary with light colour. Different spectra may therefore be applied to reduce negative impacts. We used a unique set-up of eight field sites to study the response of bats to three different experimental light spectra in an otherwise dark and undisturbed natural habitat. We measured activity of three bat species groups around transects with light posts emitting white, green and red light with an intensity commonly used to illuminate countryside roads. The results reveal a strong and spectrum-dependent response for the slow-flying Myotis and Plecotus and more agile Pipistrellus species, but not for Nyctalus and Eptesicus species. Plecotus and Myotis species avoided white and green light, but were equally abundant in red light and darkness. The agile, opportunistically feeding Pipistrellus species were significantly more abundant around white and green light, most likely because of accumulation of insects, but equally abundant in red illuminated transects compared to dark control. Forest-dwelling Myotis and Plecotus species and more synanthropic Pipistrellus species are thus least disturbed by red light. Hence, in order to limit the negative impact of light at night on bats, white and green light should be avoided in or close to natural habitat, but red lights may be used if illumination is needed.
    https://doi.org/10.1098/rspb.2017.0075
  • Frontiers in Ecology and Evolution
    30-05-2017

    Artificial Light at Night Reduces Daily Energy Expenditure in Breeding Great Tits (Parus major)

    Anouk Welbers, Natalie van Dis, Annemieke Kolvoort, Jenny Ouyang, Marcel E. Visser, Kamiel Spoelstra, Davide Dominoni
    The ecological impact of artificial light at night (ALAN) is an increasingly recognized process that accompanies expanding urbanization. Yet, we have limited knowledge on the impact of ALAN on wild species, and on the potential to mitigate any negative effects by using different light sources and colors. In birds, effects of ALAN on activity levels are reported for several species and, hence, their daily energy expenditure (DEE) may be affected. DEE is a potent mediator of life-history trade-offs and fitness and thus an important aspect to consider when examining the potential long-term ecological effects of ALAN. Previous work has suggested that birds exposed to ALAN show higher levels of provisioning and nocturnal activity, suggesting that white ALAN increases DEE. Other factors regulating DEE, such as provisioning behavior and food availability, might also respond to ALAN and thus indirectly affect DEE. We tested the hypothesis that ALAN increases DEE using an experimental setup where four previously unlit transects were illuminated with either white, green, or red LED light, or left dark as a control treatment. This setup was replicated in eight locations across the Netherlands. We measured DEE of our focal species, the great tit (Parus major), using a novel doubly labeled water technique that uses breath rather than blood samples. Contrary to our expectations, birds feeding their offspring under white and green ALAN showed lower DEE compared to birds in the control dark treatment. Differences in chick provisioning activity did not explain this result, as neither visit rates nor daily activity timing was affected by light treatment. However, food availability under white and green light was much higher compared to red light and the dark control. This difference strongly suggests that the lower DEE under white and green ALAN sites is a consequence of higher food availability in these treatments. This result shows that there can be positive, indirect effects of ALAN for breeding song birds which may balance against the negative direct effects shown in previous studies.
    https://doi.org/10.3389/fevo.2017.00055
  • Journal of Avian Biology
    15-03-2017

    Early arrival is not associated with more extra-pair fertilizations in a long-distance migratory bird

    Barbara Tomotani, Ezra Caglar, Iván De la Hera, A.C. Mateman, Marcel E. Visser
    When assessing the benefits of early arrival date of migratory birds, a hidden and often ignored component of males’ fitness is the higher chance of early-arriving birds to obtain extra-pair fertilizations. Here we investigated how extra-pair paternity might affect the relationship between male arrival date and number of fertilizations in a model study system, the European pied flycatcher Ficedula hypoleuca. For this purpose, we sampled and genotyped breeding pairs, unpaired males and offspring (including embryos from unhatched eggs when possible) of a Dutch pied flycatcher population. Detailed information on arrival date of males, egg laying date of their social mates and nest success was also recorded. Early-arriving males had early-laying females and males with early-laying females had a higher probability of siring extra-pair eggs and obtain more fertilizations. However, male arrival date alone did not correlate with the probability to gain extra-pair paternity and neither to the amount of fertilized eggs. Both early- and late-arriving males had a higher probability of losing paternity in their own nest compared to birds with an intermediate arrival date. Finally, late-arriving males were more likely to remain unpaired but, interestingly, a few of these birds obtained paternity via extra-pair copulations. Because earlier arrival date did not lead to more extra-pair fertilizations and because such relationship seems to be driven mainly by the female's laying date, we conclude that the contribution of extra-pair paternity to the overall fitness benefits of early male arrival date is relatively small.
    https://doi.org/10.1111/jav.01317
  • Royal Society Open Science
    11-01-2017

    Experimental illumination of a forest: no effects of lights of different colours on the onset of the dawn chorus in songbirds

    Arnaud Da Silva, Maaike de Jong, Roy H. A. van Grunsven, Marcel E. Visser, Bart Kempenaers, Kamiel Spoelstra
    Light pollution is increasing exponentially, but its impact on animal behaviour is still poorly understood. For songbirds, the most repeatable finding is that artificial night lighting leads to an earlier daily onset of dawn singing. Most of these studies are, however, correlational and cannot entirely dissociate effects of light pollution from other effects of urbanization. In addition, there are no studies in which the effects of different light colours on singing have been tested. Here, we investigated whether the timing of dawn singing in wild songbirds is influenced by artificial light using an experimental set-up with conventional street lights. We illuminated eight previously dark forest edges with white, green, red or no light, and recorded daily onset of dawn singing during the breeding season. Based on earlier work, we predicted that onset of singing would be earlier in the lighted treatments, with the strongest effects in the early-singing species. However, we found no significant effect of the experimental night lighting (of any colour) in the 14 species for which we obtained sufficient data. Confounding effects of urbanization in previous studies may explain these results, but we also suggest that the experimental night lighting may not have been strong enough to have an effect on singing.
    https://doi.org/10.1098/rsos.160638
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    2017

    Behavioural, ecological and evolutionary response to extreme climatic events: Challenges & directions

    Martijn van de Pol, S. Jenouvrier, J.H.C. Cornelissen, Marcel E. Visser
    More extreme climatic events (ECEs) are among the most prominent consequences of climate change. Despite a long-standing recognition of the importance of ECEs by paleo-ecologists and macro-evolutionary biologists, ECEs have only recently received a strong interest in the wider ecological and evolutionary community. However, as with many rapidly expanding fields, it lacks structure and cohesiveness, which strongly limits scientific progress. Furthermore, due to the descriptive and anecdotal nature of many ECE studies it is still unclear what the most relevant questions and long-term consequences are of ECEs. To improve synthesis, we first discuss ways to define ECEs that facilitate comparison among studies. We then argue that biologists should adhere to more rigorous attribution and mechanistic methods to assess ECE impacts. Subsequently, we discuss conceptual and methodological links with climatology and disturbance-, tipping point- and paleo-ecology. These research fields have close linkages with ECE research, but differ in the identity and/or the relative severity of environmental factors. By summarizing the contributions to this theme issue we draw parallels between behavioural, ecological and evolutionary ECE studies, and suggest that an overarching challenge is that most empirical and theoretical evidence points towards responses being highly idiosyncratic, and thus predictability being low. Finally, we suggest a roadmap based on the proposition that an increased focus on the mechanisms behind the biological response function will be crucial for increased understanding and predictability of the impacts of ECE.
    https://doi.org/10.1098/rstb.2016.0134
  • Global Change Biology
    2017

    What type of rigorous experiments are needed to investigate the impact of artificial light at night on individuals and populations?

    Jenny Ouyang, Maaike de Jong, Roy H. A. van Grunsven, Kevin D. Matson, Mark F. Haussmann, Peter Meerlo, Marcel E. Visser, Kamiel Spoelstra
    https://doi.org/10.1111/gcb.13894
  • 2017

    Phenological Shifts in Animals Under Contemporary Climate Change

    One of the best documented impacts of climate change has been on the seasonal timing, or phenology, of species. There are clear shifts in all taxonomic groups in terrestrial, aquatic, and marine environments. There is, however, ample variation in the rate at which species shift in response to warmer temperatures. As a consequence, phenological mismatches may occur, in which the phenology of one species no longer matches that of another species, for instance, in predator–prey systems. These mismatches can have an impact on the viability of populations and thereby on biodiversity.
    https://doi.org/10.1016/B978-0-12-809633-8.02301-3
  • Global Change Biology
    2017

    Restless roosts: Light pollution affects behavior, sleep, and physiology in a free-living songbird

    Jenny Ouyang, Maaike de Jong, Roy H. A. van Grunsven, Kevin D. Matson, Mark F. Haussmann, Peter Meerlo, Marcel E. Visser, Kamiel Spoelstra
    The natural nighttime environment is increasingly polluted by artificial light. Several studies have linked artificial light at night to negative impacts on human health. In free-living animals, light pollution is associated with changes in circadian, reproductive, and social behavior, but whether these animals also suffer from physiologic costs remains unknown. To fill this gap, we made use of a unique network of field sites which are either completely unlit (control), or are artificially illuminated with white, green, or red light. We monitored nighttime activity of adult great tits, Parus major, and related this activity to within-individual changes in physiologic indices. Because altered nighttime activity as a result of light pollution may affect health and well-being, we measured oxalic acid concentrations as a biomarker for sleep restriction, acute phase protein concentrations and malaria infection as indices of immune function, and telomere lengths as an overall measure of metabolic costs. Compared to other treatments, individuals roosting in the white light were much more active at night. In these individuals, oxalic acid decreased over the course of the study. We also found that individuals roosting in the white light treatment had a higher probability of malaria infection. Our results indicate that white light at night increases nighttime activity levels and sleep debt and affects disease dynamics in a free-living songbird. Our study offers the first evidence of detrimental effects of light pollution on the health of free-ranging wild animals.
    https://doi.org/10.1111/gcb.13756
  • Oikos
    12-2016

    Modeling winter moth Operophtera brumata egg phenology: nonlinear effects of temperature and developmental stage on developmental rate

    Lucia Salis, Marjolein Lof, M. Van Asch, Marcel E. Visser
    Understanding the relationship between an insect's developmental rate and temperature is crucial to forecast insect phenology under climate change. In the winter moth Operophtera brumata timing of egg-hatching has severe fitness consequences on growth and reproduction as egg-hatching has to match bud burst of the host tree. In the winter moth, as in many insect species, egg development is strongly affected by ambient temperatures. Here we use laboratory experiments to show for the first time that the effect of temperature on developmental rate depends on the stage of development of the eggs. Building on this experimental finding, we present a novel physiological model to describe winter moth egg development in response to temperature. Our model, a modification of the existing Sharpe-Schoolfield biophysical model, incorporates the effect of developmental stage on developmental rate. Next we validate this model using a 13-year data-set from winter moth eggs kept under ambient conditions and compared this validation with a degree day model and with the Sharpe-Schoolfield model, which lacks the interaction between temperature and developmental stage on developmental rate. We show that accounting for the interaction between temperature and developmental stage improved the predictive power of the model and contributed to our understanding of annual variation in winter moth egg phenology. As climate change leads to unequal changes in temperatures throughout the year, a description of insect development in response to realistic patterns of temperature rather than an invariable degree-day approach will help us to better predict future responses of insect phenology, and thereby insect fitness, to climate change.This article is protected by copyright. All rights reserved.
    https://doi.org/10.1111/oik.03257
  • General and Comparative Endocrinology
    01-09-2016

    Temperature-induced variation in yolk androgen and thyroid hormone levels in avian eggs

    Suvi Ruuskanen, Ton G.G. Groothuis, Sonja Schaper, Veerle M. Darras, Bonnie de Vries, Marcel E. Visser
    Abstract Global warming has substantially changed the environment, but the mechanisms to cope with these changes in animals, including the role of maternal effects, are poorly understood. Maternal effects via hormones deposited in eggs, have important environment-dependent effects on offspring development and fitness: thus females are expected to adjust these hormones to the environment, such as the ambient temperature. Longer-term temperature variation could function as a cue, predicting chick rearing conditions to which yolk hormone levels are adjusted, while short-term temperature variation during egg formation may causally affect hormone transfer to eggs. We studied the effects of ambient temperature on yolk androgens (testosterone and androstenedione) and thyroid hormones (thyroxine and triiodothyronine) in great tits (Parus major) using data from unmanipulated clutches from a wild population and from aviary birds (ad libitum food) exposed to different experimental temperature treatments during five years. Both in the wild and in captivity, longer-term pre-laying ambient temperature was not associated with clutch mean yolk hormone levels, while the way androstenedione and thyroxine levels varied across the laying sequence did associate with pre-laying temperature in the wild. Yolk testosterone levels were positively correlated with short-term temperature (during yolk formation) changes within clutches in both wild and captivity. We also report, for the first time in a wild bird, that yolk thyroxine levels correlated with a key environmental factor: thyroxine levels were negatively correlated with ambient temperature during egg formation. Thus, yolk hormone levels, especially testosterone, seem to be causally affected by ambient temperature. These short-term effects might reflect physiological changes in females with changes in ambient temperature. The adaptive value of the variation with ambient temperatures pre-laying or during egg formation should be studied with hormone manipulations in different thermal environments.
    https://doi.org/10.1016/j.ygcen.2016.05.026
  • PLoS One
    29-06-2016

    Do wild great tits avoid exposure to light at night?

    Maaike de Jong, Jenny Ouyang, Roy H. A. van Grunsven, Marcel E. Visser, Kamiel Spoelstra
    Studies of wild populations have provided important insights into the effects of artificial light at night on organisms, populations and ecosystems. However, in most studies the exact amount of light at night individuals are exposed to remains unknown. Individuals can potentially control their nighttime light exposure by seeking dark spots within illuminated areas. This uncertainty makes it difficult to attribute effects to a direct effect of light at night, or to indirect effects, e.g., via an effect of light at night on food availability. In this study, we aim to quantify the nocturnal light exposure of wild birds in a previously dark forest-edge habitat, experimentally illuminated with three different colors of street lighting, in comparison to a dark control. During two consecutive breeding seasons, we deployed male great tits (Parus major) with a light logger measuring light intensity every five minutes over a 24h period. We found that three males from pairs breeding in brightly illuminated nest boxes close to green and red lamp posts, were not exposed to more artificial light at night than males from pairs breeding further away. This suggests, based on our limited sample size, that these males could have been avoiding light at night by choosing a roosting place with a reduced light intensity. Therefore, effects of light at night previously reported for this species in our experimental set-up might be indirect. In contrast to urban areas where light is omnipresent, bird species in non-urban areas may evade exposure to nocturnal artificial light, thereby avoiding direct consequences of light at night.
    https://doi.org/10.1371/journal.pone.0157357
  • Biological Journal of the Linnean Society
    19-05-2016

    Low but contrasting neutral genetic differentiation shaped by winter temperature in European great tits.

    M. Lemoine, K. Lucek, C. Perrier, V. Saladin, F. Adriaensen, E. Barba, E.J. Belda, A. Charmantier, M. Cichoń, T. Eeva, A. Grégoire, C.A. Hinde, A. Johnsen, J. Komdeur, R. Mänd, E. Matthysen, A.C. Norte, N. Pitala, Ben C. Sheldon, T. Slagsvold, J.M. Tinbergen, J. Török, R. Ubels, Kees van Oers, Marcel E. Visser, Blandine Doligez, Heinz Richner
    Gene flow is usually thought to reduce genetic divergence and impede local adaptation by homogenising gene pools between populations. However, evidence for local adaptation and phenotypic differentiation in highly mobile species, experiencing high levels of gene flow, is emerging. Assessing population genetic structure at different spatial scales is thus a crucial step towards understanding mechanisms underlying intraspecific differentiation and diversification. Here, we studied the population genetic structure of a highly mobile species – the great tit Parus major – at different spatial scales. We analysed 884 individuals from 30 sites across Europe including 10 close-by sites (< 50 km), using 22 microsatellite markers. Overall we found a low but significant genetic differentiation among sites (FST = 0.008). Genetic differentiation was higher, and genetic diversity lower, in south-western Europe. These regional differences were statistically best explained by winter temperature. Overall, our results suggest that great tits form a single patchy metapopulation across Europe, in which genetic differentiation is independent of geographical distance and gene flow may be regulated by environmental factors via movements related to winter severity. This might have important implications for the evolutionary trajectories of sub-populations, especially in the context of climate change, and calls for future investigations of local differences in costs and benefits of philopatry at large scales.
    https://doi.org/10.1111/bij.12745
  • Hormones and Behavior
    05-2016

    Effects of experimentally manipulated yolk thyroid hormone levels on offspring development in a wild bird species

    Suvi Ruuskanen, Veerle M. Darras, Marcel E. Visser, Ton G.G. Groothuis
    Abstract Maternal effects are a crucial mechanism in a wide array of taxa to generate phenotypic variation, thereby affecting offspring development and fitness. Maternally derived thyroid hormones (THs) are known to be essential for offspring development in mammalian and fish models, but have been largely neglected in avian studies, especially in respect to natural variation and an ecological context. We studied, for the first time in a wild species and population, the effects of maternally derived THs on offspring development, behavior, physiology and fitness-related traits by experimental elevation of thyroxine and triiodothyronine in ovo within the physiological range in great tits (Parus major). We found that elevated yolk TH levels had a sex-specific effect on growth, increasing male and decreasing female growth, relative to controls, and this effect was similar throughout the nestling period. Hatching or fledging success, motor coordination behavior, stress reactivity and resting metabolic rate were not affected by the TH treatment. We conclude that natural variation in maternally derived THs may affect some offspring traits in a wild species. As this is the first study on yolk thyroid hormones in a wild species and population, more such studies are needed to investigate its effects on pre-hatching development, and juvenile and adult fitness before generalizations on the importance of maternally derived yolk thyroid hormones can be made. However, this opens a new, interesting avenue for further research in the field of hormone mediated maternal effects.
    https://doi.org/10.1016/j.yhbeh.2016.03.006
  • Trends in Ecology & Evolution
    02-2016

    Solutions for Archiving Data in Long-Term Studies

    James A Mills, Céline Teplitsky, Beatriz Arroyo, Anne Charmantier, Peter H Becker, Tim R Birkhead, Pierre Bize, Daniel T Blumstein, Christophe Bonenfant, Stan Boutin, Andrey Bushuev, Emmanuelle Cam, Andrew Cockburn, Steeve D Côté, John C Coulson, Francis Daunt, N.J. Dingemanse, Blandine Doligez, Hugh Drummond, Richard H M Espie, Marco Festa-Bianchet, Francesca D Frentiu, John W Fitzpatrick, Robert W Furness, Gilles Gauthier, Peter R Grant, Michael Griesser, Lars Gustafsson, Bengt Hansson, Michael P Harris, Frédéric Jiguet, Petter Kjellander, Erkki Korpimäki, Charles J Krebs, Luc Lens, John D C Linnell, Matthew Low, Andrew McAdam, Antoni Margalida, Juha Merilä, Anders P. Møller, Shinichi Nakagawa, Jan-Åke Nilsson, Ian C T Nisbet, Arie Van Noordwijk, Daniel Oro, Tomas Pärt, Fanie Pelletier, Jaime Potti, Benoit Pujol, Denis Réale, Robert F Rockwell, Yan Ropert-Coudert, Alexandre Roulin, Christophe Thébaud, James S Sedinger, Jon E Swenson, Marcel E. Visser, Sarah Wanless, David F Westneat, Alastair J Wilson, Andreas Zedrosser
    https://doi.org/10.1016/j.tree.2015.12.004
  • Evolution
    2016

    Genetic variation in variability: phenotypic variability of fledging weight and its evolution in a songbird population

    HA Mulder, Phillip Gienapp, Marcel E. Visser
    Variation in traits is essential for natural selection to operate and genetic and environmental effects can contribute to this phenotypic variation. From domesticated populations, we know that families can differ in their level of within-family variance, which leads to the intriguing situation that within-family variance can be heritable. For offspring traits, such as birth weight, this implies that within-family variance in traits can vary among families and can thus be shaped by natural selection. Empirical evidence for this in wild populations is however lacking. We investigated whether within-family variance in fledging weight is heritable in a wild great tit (Parus major) population and whether these differences are associated with fitness. We found significant evidence for genetic variance in within-family variance. The genetic coefficient of variation (GCV) was 0.18 and 0.25, when considering fledging weight a parental or offspring trait, respectively. We found a significant quadratic relationship between within-family variance and fitness: families with low or high within-family variance had lower fitness than families with intermediate within-family variance. Our results show that within-family variance can respond to selection and provides evidence for stabilizing selection on within-family variance.
    https://doi.org/10.1111/evo.13008
  • Nature Communications
    2016

    Evolutionary signals of selection on cognition from the great tit genome and methylome

    Veronika Laine, T.I. Gossmann, K.M. Schachtschneider, C.J. Garroway, O. Madsen, Koen Verhoeven, Victor de Jager, H-J. Megens, W.C. Warren, P. Minx, R.P.M.A. Crooijmans, P. Corcoran, Ben C. Sheldon, J. Slate, K. Zeng, Kees van Oers, Marcel E. Visser, M.A.M. Groenen
    For over 50 years, the great tit (Parus major) has been a model species for research in evolutionary, ecological and behavioural research; in particular, learning and cognition have been intensively studied. Here, to provide further insight into the molecular mechanisms behind these important traits, we de novo assemble a great tit reference genome and whole-genome re-sequence another 29 individuals from across Europe. We show an overrepresentation of genes related to neuronal functions, learning and cognition in regions under positive selection, as well as increased CpG methylation in these regions. In addition, great tit neuronal non-CpG methylation patterns are very similar to those observed in mammals, suggesting a universal role in neuronal epigenetic regulation which can affect learning-, memory- and experience-induced plasticity. The high-quality great tit genome assembly will play an instrumental role in furthering the integration of ecological, evolutionary, behavioural and genomic approaches in this model species.
    https://doi.org/10.1038/ncomms10474
  • Evolution
    2016

    Testing for biases in selection on avian reproductive traits and partitioning direct and indirect selection using quantitative genetic models

    Thomas Reed, Phillip Gienapp, Marcel E. Visser
    ey life history traits such as breeding time and clutch size are frequently both heritable and under directional selection, yet many studies fail to document micro-evolutionary responses. One general explanation is that selection estimates are biased by the omission of correlated traits that have causal effects on fitness, but few valid tests of this exist. Here we show, using a quantitative genetic framework and six decades of life-history data on two free-living populations of great tits Parus major, that selection estimates for egg-laying date and clutch size are relatively unbiased. Predicted responses to selection based on the Robertson-Price Identity were similar to those based on the multivariate breeder's equation, indicating that unmeasured covarying traits were not missing from the analysis. Changing patterns of phenotypic selection on these traits (for laying date, linked to climate change) therefore reflect changing selection on breeding values, and genetic constraints appear not to limit their independent evolution. Quantitative genetic analysis of correlational data from pedigreed populations can be a valuable complement to experimental approaches to help identify whether apparent associations between traits and fitness are biased by missing traits, and to parse the roles of direct versus indirect selection across a range of environments.
    https://doi.org/10.1111/evo.13017
  • Proceedings of the Royal Society B-Biological Sciences
    2016

    Climate change relaxes the time constraints for late-born offspring in a long-distance migrant

    Barbara Tomotani, Phillip Gienapp, Domien G. M. Beersma, Marcel E. Visser
    Animals in seasonal environments need to fit their annual-cycle stages, such as moult and migration, in a tight schedule. Climate change affects the phenology of organisms and causes advancements in timing of these annual-cycle stages but not necessarily at the same rates. For migratory birds, this can lead to more severe or more relaxed time constraints in the time from fledging to migration, depending on the relative shifts of the different stages. We tested how a shift in hatch date, which has advanced due to climate change, impacts the organization of the birds' whole annual cycle. We experimentally advanced and delayed the hatch date of pied flycatcher chicks in the field and then measured the timing of their annual-cycle stages in a controlled laboratory environment. Hatch date affected the timing of moult and pre-migratory fattening, but not migration. Early-born birds hence had a longer time to fatten up than late-born ones; the latter reduced their interval between onset of fattening and migration to be able to migrate at the same time as the early-born birds. This difference in time constraints for early- and late-born individuals may explain why early-born offspring have a higher probability to recruit as a breeding bird. Climate change-associated advancements of avian egg-lay dates, which in turn advances hatch dates, can thus reduce the negative fitness consequences of reproducing late, thereby reducing the selection for early egg-laying migratory birds.
    https://doi.org/10.1098/rspb.2016.1366
  • Nature Communications
    2016

    Demographic routes to variability and regulation in bird populations

    Bernt-Erik Sæther, Vidar Grøtan, Steinar Engen, Tim Coulson, Peter R Grant, Marcel E. Visser, Jon E Brommer, B Rosemary Grant, Lars Gustafsson, Ben J Hatchwell, Kurt Jerstad, Patrik Karell, Hannu Pietiäinen, Alexandre Roulin, Ole W Røstad, Henri Weimerskirch
    There is large interspecific variation in the magnitude of population fluctuations, even among closely related species. The factors generating this variation are not well understood, primarily because of the challenges of separating the relative impact of variation in population size from fluctuations in the environment. Here, we show using demographic data from 13 bird populations that magnitudes of fluctuations in population size are mainly driven by stochastic fluctuations in the environment. Regulation towards an equilibrium population size occurs through density-dependent mortality. At small population sizes, population dynamics are primarily driven by environment-driven variation in recruitment, whereas close to the carrying capacity K, variation in population growth is more strongly influenced by density-dependent mortality of both juveniles and adults. Our results provide evidence for the hypothesis proposed by Lack that population fluctuations in birds arise from temporal variation in the difference between density-independent recruitment and density-dependent mortality during the non-breeding season.
    https://doi.org/10.1038/ncomms12001
  • Heredity
    2016

    Heritable variation in maternally derived yolk androgens, thyroid hormones and immune factors

    Suvi Ruuskanen, Phillip Gienapp, T.G.G. Groothuis, Sonja Schaper, Veerle M. Darras, Cheila Pereira, B. de Vries, Marcel E. Visser
    Maternal reproductive investment can critically influence offspring phenotype, and thus these maternal effects are expected to be under strong natural selection. Knowledge on the extent of heritable variation in the physiological mechanisms underlying maternal effects is however limited. In birds, resource allocation to eggs is a key mechanism for mothers to affect their offspring and different components of the egg may or may not be independently adjusted. We studied the heritability of egg components and their genetic and phenotypic covariation in great tits (Parus major), using captive-bred full siblings of wild origin. Egg mass, testosterone (T) and androstenedione (A4) hormone concentrations showed moderate heritability, in agreement with earlier findings. Interestingly, yolk triiodothyronine hormone (T3), but not its precursor, thyroxine hormone (T4), concentration was heritable. An immune factor, albumen lysozyme, showed moderate heritability, but yolk immunoglobulins (IgY) did not. The genetic correlation estimates were moderate but statistically nonsignificant; a trend for a positive genetic correlation was found between A4 and egg mass, T and lysozyme and IgY and lysozyme, respectively. Interestingly, phenotypic correlations were found only between A4 and T, and T4 and T3, respectively. Given that these egg components are associated with fitness-related traits in the offspring (and mother), and that we show that some components are heritable, it opens the possibility that natural selection may shape the rate and direction of phenotypic change via egg composition.
    https://doi.org/10.1038/hdy.2016.49
  • Journal of Avian Biology
    2016

    Experimental manipulation of food availability leads to short-term intra-clutch adjustment in egg mass but not in yolk androgen or thyroid hormones.

    Suvi Ruuskanen, V.M. Darras, B. de Vries, Marcel E. Visser, T.G.G. Groothuis
    In birds, mothers can affect their offspring's phenotype and thereby survival via egg composition. It is not well known to what extent and time-scales environmental variation in resource availability, either via resource constrains or adaptive adjustment to predicted rearing conditions, influences maternal effects. We experimentally studied whether egg and yolk mass and yolk hormone levels respond to short-term changes in food availability during laying in wild great tits (Parus major). Our treatment groups were: 1) food supplementation (mealworms) from the 1st until the last egg; 2) food supplementation from the 1st first until the 5th egg, where the effect of cessation of the supplementary food treatment could also be studied; 3) no food supplementation (controls). We analysed both nutritional resources (egg, yolk and albumen mass), and the important developmental signals, yolk androgens (testosterone and androstenedione), and for the first time in a wild population, yolk thyroid hormones (thyroxine and 3,5,3’-triiodothyronine). Egg mass is a costly resource for females, androgens most likely non-costly signals, whereas thyroid hormones may be costly signals, requiring environmental iodine. In the food supplemented group egg, yolk and albumen mass increased rapidly relative to controls and when food supplementation was halted, egg and albumen mass decreased, indicating rapid responses to resource availability. Yolk androgen and thyroid hormone levels were not affected by food supplementation during laying. Thyroxine showed an increase over the laying sequence and its biological meaning needs further study. The rapid changes in egg mass to variation in within-clutch food availability suggest energetic/protein/nutrient constrains on egg formation. The lack of a response in yolk hormones suggest that perhaps in this species the short-term changes in resource availability during egg laying do not predict offspring rearing conditions, or (for thyroid hormones) do not cause systemic changes in circulating hormones, and hence do not affect maternal signaling.
    https://doi.org/10.1111/jav.00728
  • Physiology & Behavior
    2016

    Dose-dependent responses of avian daily rhythms to artificial light at night

    Maaike de Jong, Lizanne Jeninga, Jenny Ouyang, Kees van Oers, Kamiel Spoelstra, Marcel E. Visser
    Recent studies have shown that animals are affected by night-time light exposure. Light is a continuous variable, but our knowledge on how individuals react to different light intensities during the night is limited. We therefore determined the relationship between night light intensity and the behaviour and physiology of great tits (Parus major). We measured daily activity patterns and melatonin levels in 35 males exposed to five different light intensities and found strong, dose-dependent effects. Activity onset was increasingly advanced, and activity offset delayed with higher light intensities. Furthermore, night-time activity increased and melatonin levels measured at midnight decreased with higher intensities. In this experimental study, we demonstrate for the first time dose-dependent effects of artificial light at night on birds' daily activity patterns and melatonin levels. Our results imply that these effects are not limited to a certain threshold, but emerge even when nocturnal light levels are slightly increased. However, in a natural area, these effects may be limited as artificial light levels are commonly low; light intensities drop rapidly with distance from a light source and birds can avoid exposure to light at night. Future studies should thus focus on examining the impact of different intensities of light at night in the wild.
    https://doi.org/10.1016/j.physbeh.2015.12.012
  • Proceedings of the Royal Society B-Biological Sciences
    2016

    Evidence for r- and K-selection in a wild bird population: a reciprocal link between ecology and evolution.

    S.A. Saether, Marcel E. Visser, V. Grotan, S. Engen
    Understanding the variation in selection pressure on key life-history traits is crucial in our rapidly changing world. Density is rarely considered as a selective agent. To study its importance, we partition phenotypic selection in fluctuating environments into components representing the population growth rate at low densities and the strength of density dependence, using a new stochastic modelling framework. We analysed the number of eggs laid per season in a small song-bird, the great tit, and found balancing selection favouring large clutch sizes at small population densities and smaller clutches in years with large populations. A significant interaction between clutch size and population size in the regression for the Malthusian fitness reveals that those females producing large clutch sizes at small population sizes also are those that show the strongest reduction in fitness when population size is increased. This provides empirical support for ongoing r- and K-selection in this population, favouring phenotypes with large growth rates r at small population sizes and phenotypes with high competitive skills when populations are close to the carrying capacity K. This selection causes long-term fluctuations around a stable mean clutch size caused by variation in population size, implying that r- and K-selection is an important mechanism influencing phenotypic evolution in fluctuating environments. This provides a general link between ecological dynamics and evolutionary processes, operating through a joint influence of density dependence and environmental stochasticity on fluctuations in population size.
    https://doi.org/10.1098/rspb.2015.2411
  • Ecology
    2016

    Density dependence in an age-structured population of great tits: identifying the critical age classes

    M. Gamelon, V. Grotan, S. Engen, E. Bjørkvoll, Marcel E. Visser, Bernt-Erik Sæther
    Classical approaches for the analyses of density dependence assume that all the individuals in a population equally respond and equally contribute to density dependence. However, in age-structured populations, individuals of different ages may differ in their responses to changes in population size and how they contribute to density dependence affecting the growth rate of the whole population. Here, we apply the concept of critical age classes, i.e., a specific scalar function that describes how one or a combination of several age classes affect the demographic rates negatively, in order to examine how total density dependence acting on the population growth rate depends on the age-specific population sizes. In a 38-year dataset of an age-structured great tit (Parus major) population, we find that the age classes including the youngest breeding females were the critical age classes for density regulation. These age classes correspond to new breeders that attempt to take a territory and that have the strongest competitive effect on other breeding females. They strongly affected population growth rate and reduced recruitment and survival rates of all breeding females. We also show that depending on their age class, females may differently respond to varying density. In particular, the negative effect of the number of breeding females was stronger on recruitment rate of the youngest breeding females. These findings question the classical assumptions that all the individuals of a population can be treated as having an equal contribution to density regulation and that the effect of the number of individuals is age independent. Our results improve our understanding of density regulation in natural populations.
    https://doi.org/10.1002/ecy.1442
  • Molecular Ecology
    12-2015

    Replicated analysis of the genetic architecture of quantitative traits in two wild great tit populations.

    A.W. Santure, J. Poissant, I. de Cauwer, Kees van Oers, M.R. Robinson, J.L. Quinn, M.A.M. Groenen, Marcel E. Visser, Ben C. Sheldon, J. Slate
    Currently, there is much debate on the genetic architecture of quantitative traits in wild populations. Is trait variation influenced by many genes of small effect or by a few genes of major effect? Where is additive genetic variation located in the genome? Do the same loci cause similar phenotypic variation in different populations? Great tits (Parus major) have been studied extensively in long-term studies across Europe and consequently are considered an ecological ‘model organism’. Recently, genomic resources have been developed for the great tit, including a custom SNP chip and genetic linkage map. In this study, we used a suite of approaches to investigate the genetic architecture of eight quantitative traits in two long-term study populations of great tits—one in the Netherlands and the other in the United Kingdom. Overall, we found little evidence for the presence of genes of large effects in either population. Instead, traits appeared to be influenced by many genes of small effect, with conservative estimates of the number of contributing loci ranging from 31 to 310. Despite concordance between population-specific heritabilities, we found no evidence for the presence of loci having similar effects in both populations. While population-specific genetic architectures are possible, an undetected shared architecture cannot be rejected because of limited power to map loci of small and moderate effects. This study is one of few examples of genetic architecture analysis in replicated wild populations and highlights some of the challenges and limitations researchers will face when attempting similar molecular quantitative genetic studies in free-living populations
    https://doi.org/10.1111/mec.13452
  • Proceedings of the Royal Society B-Biological Sciences
    22-05-2015

    Testing for effects of climate change on competitive relationships and coexistence between two bird species

    Nils Chr. Stenseth, Joel M. Durant, Mike S. Fowler, Erik Matthysen, Frank Adriaensen, Niclas Jonzen, Kung-Sik Chan, Hai Liu, Jenny De Laet, Ben C. Sheldon, Marcel E. Visser, Andre A. Dhondt
    Climate change is expected to have profound ecological effects, yet shifts in competitive abilities among species are rarely studied in this context. Blue tits (Cyanistes caeruleus) and great tits (Parus major) compete for food and roosting sites, yet coexist across much of their range. Climate change might thus change the competitive relationships and coexistence between these two species. Analysing four of the highest-quality, long-term datasets available on these species across Europe, we extend the textbook example of coexistence between competing species to include the dynamic effects of long-term climate variation. Using threshold time-series statistical modelling, we demonstrate that long-term climate variation affects species demography through different influences on density-dependent and density-independent processes. The competitive interaction between blue tits and great tits has shifted in one of the studied sites, creating conditions that alter the relative equilibrium densities between the two species, potentially disrupting long-term coexistence. Our analyses show that long-term climate change can, but does not always, generate local differences in the equilibrium conditions of spatially structured species assemblages. We demonstrate how long-term data can be used to better understand whether (and how), for instance, climate change might change the relationships between coexisting species. However, the studied populations are rather robust against competitive exclusion.
    https://doi.org/10.1098/rspb.2014.1958
  • PLoS Biology
    07-04-2015

    Effects of Spring Temperatures on the Strength of Selection on Timing of Reproduction in a Long-Distance Migratory Bird

    Marcel E. Visser, Phillip Gienapp, Arild Husby, Michael Morrisey, Iván De la Hera, F. Pulido, Christiaan Both

    A 31-year study of pied flycatchers shows that it is the temperature at arrival when the offspring return to breed up to two years later that drives selection on breeding time.

    Climate change has differentially affected the timing of seasonal events for interacting trophic levels, and this has often led to increased selection on seasonal timing. Yet, the environmental variables driving this selection have rarely been identified, limiting our ability to predict future ecological impacts of climate change. Using a dataset spanning 31 years from a natural population of pied flycatchers (Ficedula hypoleuca), we show that directional selection on timing of reproduction intensified in the first two decades (1980–2000) but weakened during the last decade (2001–2010). Against expectation, this pattern could not be explained by the temporal variation in the phenological mismatch with food abundance. We therefore explored an alternative hypothesis that selection on timing was affected by conditions individuals experience when arriving in spring at the breeding grounds: arriving early in cold conditions may reduce survival. First, we show that in female recruits, spring arrival date in the first breeding year correlates positively with hatch date; hence, early-hatched individuals experience colder conditions at arrival than late-hatched individuals. Second, we show that when temperatures at arrival in the recruitment year were high, early-hatched young had a higher recruitment probability than when temperatures were low. We interpret this as a potential cost of arriving early in colder years, and climate warming may have reduced this cost. We thus show that higher temperatures in the arrival year of recruits were associated with stronger selection for early reproduction in the years these birds were born. As arrival temperatures in the beginning of the study increased, but recently declined again, directional selection on timing of reproduction showed a nonlinear change. We demonstrate that environmental conditions with a lag of up to two years can alter selection on phenological traits in natural populations, something that has important implications for our understanding of how climate can alter patterns of selection in natural populations.

    https://doi.org/10.1371/journal.pbio.1002120
  • Philosophical Transactions of the Royal Society B
    2015

    Effects of nocturnal illumination on life-history decisions and fitness in two wild songbird species

    Maaike de Jong, Jenny Ouyang, Arnaud Da Silva, Roy H. A. van Grunsven, Bart Kempenaers, Marcel E. Visser, Kamiel Spoelstra
    The effects of artificial night lighting on animal behaviour and fitness are largely unknown. Most studies report short-term consequences in locations that are also exposed to other anthropogenic disturbance. We know little about how the effects of nocturnal illumination vary with different light colour compositions. This is increasingly relevant as the use of LED lights becomes more common, and LED light colour composition can be easily adjusted. We experimentally illuminated previously dark natural habitat with white, green and red light, and measured the effects on life-history decisions and fitness in two free-living songbird species, the great tit (Parus major) and pied flycatcher (Ficedula hypoleuca) in two consecutive years. In 2013, but not in 2014, we found an effect of light treatment on lay date, and of the interaction of treatment and distance to the nearest lamp post on chick mass in great tits but not in pied flycatchers. We did not find an effect in either species of light treatment on breeding densities, clutch size, probability of brood failure, number of fledglings and adult survival. The finding that light colour may have differential effects opens up the possibility to mitigate negative ecological effects of nocturnal illumination by using different light spectra. artificial light at nightlight spectralife-historyfitnessParus majorFicedula hypoleucaFootnotesOne contribution of 14 to a theme issue ‘The biological impacts of artificial light at night: from molecules to communities’.© 2015 The Author(s) Published by the Royal Society. All rights reserved.
    https://doi.org/10.1098/rstb.2014.0128
  • Proceedings of the Royal Society B-Biological Sciences
    2015

    Disrupted seasonal biology impacts health, food security, and ecosystems: a call for integrated research

    T.J. Stevenson, Marcel E. Visser, W. Arnold, P Barrett, S. Biello, A. Dawson, D.L. Denlinger, Davide Dominoni, F.J. Ebling, S. Elton, N. Evans, H.M. Ferguson, R.G. Foster, M. Hau, D.T. Haydon, D.G. Hazlerigg, P. Heideman, J.G.C. Hopcraft, N.N. Jonsson, N. Kronfeld-Schor, V. Kumar, G.A. Lincoln, R. MacLeod, S.A.M. Martin, M. Martinez-Bakker, R.J. Nelson, Thomas Reed, J.E. Robinso, D. Rock, W.J. Schwartz, I. Steffan-Dewenter, E. Tauber, S.J. Thackeray, C. Umstatter, T. Yoshimura, B. Helm
    The rhythm of life on earth is shaped by seasonal changes in the environment. Plants and animals show profound annual cycles in physiology, health, morphology, behaviour and demography in response to environmental cues. Seasonal biology impacts ecosystems and agriculture, with consequences for humans and biodiversity. Human populations show robust annual rhythms in health and well-being, and the birth month can have lasting effects that persist throughout life. This review emphasizes the need for a better understanding of seasonal biology against the backdrop of its rapidly progressing disruption through climate change, human lifestyles and other anthropogenic impact. Climate change is modifying annual rhythms to which numerous organisms have adapted, with potential consequences for industries relating to health, ecosystems and food security. Disconcertingly, human lifestyles under artificial conditions of eternal summer provide the most extreme example for disconnect from natural seasons, making humans vulnerable to increased morbidity and mortality. In this review, we introduce scenarios of seasonal disruption, highlight key aspects of seasonal biology and summarize from biomedical, anthropological, veterinary, agricultural and environmental perspectives the recent evidence for seasonal desynchronization between environmental factors and internal rhythms. Because annual rhythms are pervasive across biological systems, they provide a common framework for trans-disciplinary research.
    https://doi.org/10.1098/rspb.2015.1453
  • Evolution
    2015

    Estimating the variation, autocorrelation, and environmental sensitivity of phenotypic selection

    Luis-Miguel Chevin, Marcel E. Visser, Jarle Tufto
    Despite considerable interest in temporal and spatial variation of phenotypic selection, very few methods allow quantifying this variation while correctly accounting for the error variance of each individual estimate. Furthermore, the available methods do not estimate the autocorrelation of phenotypic selection, which is a major determinant of eco-evolutionary dynamics in changing environments. We introduce a new method for measuring variable phenotypic selection using random regression. We rely on model selection to assess the support for stabilizing selection, and for a moving optimum that may include a trend plus (possibly autocorrelated) fluctuations. The environmental sensitivity of selection also can be estimated by including an environmental covariate. After testing our method on extensive simulations, we apply it to breeding time in a great tit population in the Netherlands. Our analysis finds support for an optimum that is well predicted by spring temperature, and occurs about 33 days before a peak in food biomass, consistent with what is known from the biology of this species. We also detect autocorrelated fluctuations in the optimum, beyond those caused by temperature and the food peak. Because our approach directly estimates parameters that appear in theoretical models, it should be particularly useful for predicting eco-evolutionary responses to environmental change.
    https://doi.org/10.1111/evo.12741
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    2015

    Experimental illumination of natural habitat—an experimental set-up to assess the direct and indirect ecological consequences of artificial light of different spectral composition

    Kamiel Spoelstra, Roy H. A. van Grunsven, Maurice Donners, Phillip Gienapp, Martinus E. Huigens, Roy Slaterus, Frank Berendse, Marcel E. Visser, Elmar M. Veenendaal
    Artificial night-time illumination of natural habitats has increased dramatically over the past few decades. Generally, studies that assess the impact of artificial light on various species in the wild make use of existing illumination and are therefore correlative. Moreover, studies mostly focus on short-term consequences at the individual level, rather than long-term consequences at the population and community level—thereby ignoring possible unknown cascading effects in ecosystems. The recent change to LED lighting has opened up the exciting possibility to use light with a custom spectral composition, thereby potentially reducing the negative impact of artificial light. We describe here a large-scale, ecosystem-wide study where we experimentally illuminate forest-edge habitat with different spectral composition, replicated eight times. Monitoring of species is being performed according to rigid protocols, in part using a citizen-science-based approach, and automated where possible. Simultaneously, we specifically look at alterations in behaviour, such as changes in activity, and daily and seasonal timing. In our set-up, we have so far observed that experimental lights facilitate foraging activity of pipistrelle bats, suppress activity of wood mice and have effects on birds at the community level, which vary with spectral composition. Thus far, we have not observed effects on moth populations, but these and many other effects may surface only after a longer period of time. experimental lightingpopulation dynamicsdaily timingseasonal timingcascading effectscitizen scienceFootnotesOne contribution of 14 to a theme issue ‘The biological impacts of artificial light at night: from molecules to communities’.© 2015 The Author(s) Published by the Royal Society. All rights reserved.
    https://doi.org/10.1098/rstb.2014.0129
  • Trends in Ecology & Evolution
    2015

    Archiving primary data: solutions for long-term studies

    J.A. Mills, C. Teplitsky, B. Arroyo, A. Charmantier, P. H. Becker, T.R. Birkhead, P. Bize, D.T. Blumstein, C. Bonenfant, S. Boutin, Andrey Bushuev, E. Cam, A. Cockburn, S.D. Côté, J.C. Coulson, F. Daunt, N.J. Dingemanse, B. Doligez, H. Drummond, R.H.M. Espie, M. Festa-Bianchet, F. Frentiu, J.W. Fitzpatrick, R.W. Furness, D. Garant, G. Gauthier, P.R. Grant, M. Griesser, L. Gustafsson, B. Hansson, M.P. Harris, F. Jiguet, P. Kjellander, E. Korpimäki, C.J. Krebs, L. Lens, J.D.C. Linnell, M. Low, A. McAdam, A. Margalida, J. Merilä, Anders P. Møller, S. Nakagawa, J.-Å. Nilsson, I.C.T. Nisbet, Arie Van Noordwijk, D. Oro, T. Pärt, F. Pelletier, J. Potti, B. Pujol, D. Réale, R.F. Rockwell, Y. Ropert-Coudert, A. Roulin, C. Thébaud, J.S. Sedinger, J.E. Swenson, Marcel E. Visser, D.F. S.Wanless Westneat, A.J. Wilson, A. Zedrosser
    The recent trend for journals to require open access to primary data included in publications has been embraced by many biologists, but has caused apprehension amongst researchers engaged in long-term ecological and evolutionary studies. A worldwide survey of 73 principal investigators (Pls) with long-term studies revealed positive attitudes towards sharing data with the agreement or involvement of the PI, and 93% of PIs have historically shared data. Only 8% were in favor of uncontrolled, open access to primary data while 63% expressed serious concern. We present here their viewpoint on an issue that can have non-trivial scientific consequences. We discuss potential costs of public data archiving and provide possible solutions to meet the needs of journals and researchers.
    https://doi.org/10.1016/j.tree.2015.07.006
  • Oikos
    2015

    Density dependence and microevolution interactively determine effects of phenology mismatch on population dynamics

    Thomas Reed, Phillip Gienapp, Marcel E. Visser
    Life cycle events in plants and animals are typically adaptively tuned to anticipate predictable seasonal changes in environmental conditions or resources. Climate change is expected to affect the temporal component of species’ interactions, e.g. by creating a mismatch between a predator's breeding time (when ample food supply is critical) and the time when prey abundance is high. The demographic implications of such a mismatch remain unclear, however. Here we focussed on changes in the phenology of consumers relative to that of their food. We developed a model where reproductive output of the consumer up to offspring independence depended on mismatch and recruitment of the offspring to breeders depended on offspring density according to a Beverton–Holt function. Using a deterministic version of the model, we clarified how the effects of (constant) mismatch on equilibrium population size depended on the emergent strength of negative density dependence (DD). Using a stochastic, individual-based version, we showed that when the environment changed abruptly, the rate of population recovery was faster when heritability of seasonal timing was higher and DD was stronger. When the environment shifted continuously, the rate of decline in population size was inversely proportional to the rate of microevolution, but stronger DD slowed the rate of decline for a given heritability and thus effectively ‘bought time’ for evolutionary rescue. These results highlight the importance of negative DD, which interacts with the effects of trait heritability and stabilizing selection strength, in influencing the fate of populations experiencing environmental change. We emphasize, however, that outcomes in nature will depend crucially on the exact nature of DD, in particular whether population growth rate differences are greatest at low or high densities, highlighting the need for empirical comparisons of compensatory processes in different populations or species.
    https://doi.org/10.1111/oik.01398
  • Biology Letters
    2015

    Stressful colours: corticosterone concentrations in a free-living songbird vary with the spectral composition of experimental illumination

    Jenny Ouyang, Maaike de Jong, Michaela Hau, Marcel E. Visser, Roy H. A. van Grunsven, Kamiel Spoelstra
    Organisms have evolved under natural daily light/dark cycles for millions of years. These cycles have been disturbed as night-time darkness is increasingly replaced by artificial illumination. Investigating the physiological consequences of free-living organisms in artificially lit environments is crucial to determine whether nocturnal lighting disrupts circadian rhythms, changes behaviour, reduces fitness and ultimately affects population numbers. We make use of a unique, large-scale network of replicated field sites which were experimentally illuminated at night using lampposts emanating either red, green, white or no light to test effect on stress hormone concentrations (corticosterone) in a songbird, the great tit (Parus major). Adults nesting in white-light transects had higher corticosterone concentrations than in the other treatments. We also found a significant interaction between distance to the closest lamppost and treatment type: individuals in red light had higher corticosterone levels when they nested closer to the lamppost than individuals nesting farther away, a decline not observed in the green or dark treatment. Individuals with high corticosterone levels had fewer fledglings, irrespective of treatment. These results show that artificial light can induce changes in individual hormonal phenotype. As these effects vary considerably with light spectrum, it opens the possibility to mitigate these effects by selecting street lighting of specific spectra.
    https://doi.org/10.1098/rsbl.2015.0517
  • Genome Biology and Evolution
    2015

    The genome of the winter moth (Operophtera brumata) provides a genomic perspective on sexual dimorphism and phenology

    M. Derks, Sandra Smit, Lucia Salis, E. Schijlen, A. Bossers, A.C. Mateman, Agata Pijl, A. De Ridder, M.A.M. Groenen, Marcel E. Visser, H-J. Megens
    The winter moth (Operophtera brumata) belongs to one of the most species-rich families in Lepidoptera, the Geometridae (approx. 23,000 species). This family is of great economic importance as most species are herbivorous and capable of defoliating trees. Genome assembly of the winter moth allows the study of genes and gene families, such as the cytochrome P450 gene family, which is known to be vital in plant secondary metabolite detoxification and host plant selection. It also enables exploration of the genomic basis for female brachyptery (wing reduction), a feature of sexual dimorphism in winter moth, and for seasonal timing, a trait extensively studied in this species. Here we present a reference genome for the winter moth, the first geometrid and largest sequenced Lepidopteran genome to date (638 Mb) including a set of 16,912 predicted protein-coding genes. This allowed us to assess the dynamics of evolution on a genome wide scale using the P450 gene family. We also identified an expanded gene family potentially linked to female brachyptery, and annotated the genes involved in the circadian clock mechanism as main candidates for involvement in seasonal timing. The genome will contribute to Lepidopteran genomic resources and comparative genomics. In addition, the genome enhances our ability to understand the genetic and molecular basis of insect seasonal timing and thereby provides a reference for future evolutionary and population studies on the winter moth.
    https://doi.org/10.1093/gbe/evv145
  • Proceedings of the Royal Society B-Biological Sciences
    2014

    Why climate change will invariably alter selection pressures on phenology

    Phillip Gienapp, Thomas Reed, Marcel E. Visser
    The seasonal timing of lifecycle events is closely linked to individual fitness and hence, maladaptation in phenological traits may impact population dynamics. However, few studies have analysed whether and why climate change will alter selection pressures and hence possibly induce maladaptation in phenology. To fill this gap, we here use a theoretical modelling approach. In our models, the phenologies of consumer and resource are (potentially) environmentally sensitive and depend on two different but correlated environmental variables. Fitness of the consumer depends on the phenological match with the resource. Because we explicitly model the dependence of the phenologies on environmental variables, we can test how differential (heterogeneous) versus equal (homogeneous) rates of change in the environmental variables affect selection on consumer phenology. As expected, under heterogeneous change, phenotypic plasticity is insufficient and thus selection on consumer phenology arises. However, even homogeneous change leads to directional selection on consumer phenology. This is because the consumer reaction norm has historically evolved to be flatter than the resource reaction norm, owing to time lags and imperfect cue reliability. Climate change will therefore lead to increased selection on consumer phenology across a broad range of situations.
    https://doi.org/10.1098/rspb.2014.1611
  • Ibis
    2014

    Longitudinal data reveal ontogenetic changes in the wing morphology of a long-distance migratory bird

    Iván De la Hera, F. Pulido, Marcel E. Visser
    In migratory bird species, juveniles normally have shorter and more rounded wings than adults. The causes of this age-specific difference in wing morphology, however, are largely unknown. Here, we used longitudinal data collected over 3 years from a Pied Flycatcher Ficedula hypoleuca population to assess whether age-related differences in wing morphology are a consequence of ontogenetic changes or of selection favouring birds with longer and more pointed wings. Our study provides evidence of ontogenetic changes in wing length and shape, whereby birds grow longer and more pointed wings as they grow older. Age-dependent variation is likely to be adaptive and may partly explain age differences in spring migration phenology and breeding success.
    https://doi.org/10.1111/ibi.12112
  • Environmental Science and Pollution Research
    2014

    Large-scale geographical variation in eggshell heavy metal and calcium content in a passerine bird (Ficedula hypoleuca)

    Suvi Ruuskanen, J. Morales, T. Laaksonen, J. Moreno, R. Mateo, E. Belskii, Andrey Bushuev, A. Jarvinen, A. Kerimov, I. Krams, C. Morosinotto, R. Mand, M. Orell, A. Qvarnstrom, F.M. Slater, H. Siitari, V. Tilgar, Marcel E. Visser, W. Winkel, H. Zang, T. Eeva
    Birds have been used as bioindicators of pollution, such as toxic metals. Levels of pollutants in eggs are especially interesting, as developing birds are more sensitive to detrimental effects of pollutants than adults. Only very few studies have monitored intraspecific, large-scale variation in metal pollution across a species' breeding range. We studied large-scale geographic variation in metal levels in the eggs of a small passerine, the pied flycatcher (Ficedula hypoleuca), sampled from 15 populations across Europe. We measured 10 eggshell elements (As, Cd, Cr, Cu, Ni, Pb, Zn, Se, Sr, and Ca) and several shell characteristics (mass, thickness, porosity, and color). We found significant variation among populations in eggshell metal levels for all metals except copper. Eggshell lead, zinc, and chromium levels decreased from central Europe to the north, in line with the gradient in pollution levels over Europe, thus suggesting that eggshell can be used as an indicator of pollution levels. Eggshell lead levels were also correlated with soil lead levels and pH. Most of the metals were not correlated with eggshell characteristics, with the exception of shell mass, or with breeding success, which may suggest that birds can cope well with the current background exposure levels across Europe.
    https://doi.org/10.1007/s11356-013-2299-0
  • Heredity
    2014

    Replicated high-density genetic maps of two great tit populations reveal fine-scale genomic departures from sex-equal recombination rates

    Kees van Oers, A.W. Santure, I. de Cauwer, N.E.M. Van Bers, R.P.M.A. Crooijmans, Ben C. Sheldon, Marcel E. Visser, J. Slate, M.A.M. Groenen
    Linking variation in quantitative traits to variation in the genome is an important, but challenging task in the study of life-history evolution. Linkage maps provide a valuable tool for the unravelling of such trait−gene associations. Moreover, they give insight into recombination landscapes and between-species karyotype evolution. Here we used genotype data, generated from a 10k single-nucleotide polymorphism (SNP) chip, of over 2000 individuals to produce high-density linkage maps of the great tit (Parus major), a passerine bird that serves as a model species for ecological and evolutionary questions. We created independent maps from two distinct populations: a captive F2-cross from The Netherlands (NL) and a wild population from the United Kingdom (UK). The two maps contained 6554 SNPs in 32 linkage groups, spanning 2010 cM and 1917 cM for the NL and UK populations, respectively, and were similar in size and marker order. Subtle levels of heterochiasmy within and between chromosomes were remarkably consistent between the populations, suggesting that the local departures from sex-equal recombination rates have evolved. This key and surprising result would have been impossible to detect if only one population was mapped. A comparison with zebra finch Taeniopygia guttata, chicken Gallus gallus and the green anole lizard Anolis carolinensis genomes provided further insight into the evolution of avian karyotypes.
    https://doi.org/10.1038/hdy.2013.107
  • PLoS One
    2014

    Mate Preference of Female Blue Tits Varies with Experimental Photoperiod

    L.B. Reparaz, Kees van Oers, Marc Naguib, C. Doutrelant, Marcel E. Visser, Samuel P. Caro
    Organisms use environmental cues to time their life-cycles and among these cues, photoperiod is the main trigger of reproductive behaviours such as territory defence or song activity. Whether photoperiod is also important for another behaviour closely associated with reproduction, mate choice, is unknown. In many bird species, mate choice occurs at two different times during the annual cycle that strongly differ in daylength: in late winter when photoperiod is short and social mates are chosen, and again around egg-laying when photoperiod is longer and extra-pair mates are chosen. This duality makes the role that photoperiod plays on mate choice behaviours intriguing. We investigated the effect of photoperiod on mate choice using three experimental photoperiodic treatments (9 L:15 D, 14 L:10 D, 18 L:6 D), using blue tits (Cyanistes caeruleus) as a biological model. We show that female choice was stronger under long photoperiods. In addition, female blue tits spent significantly more time near males with long tarsi and long wings. This latter preference was only expressed under long photoperiods, suggesting that some indices of male quality only become significant to females when they are strongly photostimulated, and therefore that females could select their social and extra-pair mates based on different phenotypic traits. These results shed light on the roles that photoperiod may play in stimulating pair-bonding and in refining female selectivity for male traits.
    https://doi.org/10.1371/journal.pone.0092527
  • Journal of Avian Biology
    2013

    Variation in eggshell traits between geographically distant populations of pied flycatchers Ficedula hypoleuca

    J. Morales, Suvi Ruuskanen, T. Laaksonen, R. Mateo, E. Belskii, T. Eeva, A. Jarvinen, A. Kerimov, E. Korpimaki, I. Krams, C. Morosinotto, R. Mand, M. Orell, A. Qvarnstrom, H. Siitari, F.M. Slager, V. Tiglar, Marcel E. Visser, W. Winkel, H. Zang, J. Moreno
    The expression and impact of maternal effects may vary greatly between populations and environments. However, little is known about large-scale geographical patterns of variation in maternal deposition to eggs. In birds, as in other oviparous animals, the outermost maternal component of an egg is the shell, which protects the embryo, provides essential mineral resources and allows its interaction with the environment in the form of gas exchange. In this study, we explored variation of eggshell traits (mass, thickness, pore density and pigmentation) across 15 pied flycatcher populations at a large geographic scale. We found significant between-population variation in all eggshell traits, except in pore density, suggesting spatial variation in their adaptive benefits or in the females’ physiological limitations during egg laying. Between- population variation in shell structure was not due to geographic location (latitude and longitude) or habitat type. However, eggshells were thicker in populations that experienced higher ambient temperature during egg laying. This could be a result of maternal resource allocation to the shell being constrained under low temperatures or of an adaptation to reduce egg water loss under high temperatures. We also found that eggshell colour intensity was positively associated with biliverdin pigment concentration, shell thickness and pore density. To conclude, our findings reveal large- scale between-population variation of eggshell traits, although we found little environmental dependency in their expression. Our findings call for further studies that explore other environmental factors (e.g. calcium availability and pollution levels) and social factors like sexual selection intensity that may account for differences in shell structure between populations.
    https://doi.org/10.1111/j.1600-048X.2012.05782.x
  • Journal of Avian Biology
    2013

    Great tits provided with ad libitum food lay larger eggs when exposed to colder temperatures

    Sonja Schaper, Marcel E. Visser
    The amount of nutrients deposited into a bird egg varies both between and within clutches of the same female. Larger eggs enhance offspring traits, but as a tradeoff, laying large eggs also infers energetic costs to the female. Income breeders usually lay larger eggs later in the season, when temperatures and food availability are higher. Egg size is thus affected by the daily amount of energy available to produce an egg under cold conditions, but it is less well known in how far temperature exerts direct effects on egg size. We show that great tit females Parus major with access to ad libitum food and breeding in climate-controlled aviaries varied their egg investments. The size of an individual egg was best predicted by mean temperatures one week pre-laying, with females laying larger, rather than smaller, eggs under colder conditions. Eggs increased in size over the season, but not significantly over the laying sequence. The degree of daily temperature fluctuation did not influence egg size. In addition to a substantial between-female variation, sisters were more similar to each other than unrelated females, showing that egg size does also reflect heritable intrinsic female properties. Natural variation in egg size is thus not only determined by energy-limitation, but also due to females allocating more resources to eggs laid in colder environments, thus increasing early survival of the chicks. That the positive correlation between temperature and egg investments that is found in a natural population is reversed under ad libitum food conditions demonstrates that wild great tits tradeoff own condition with survival prospects of their chicks as a function of available food, not ambient temperature.
    https://doi.org/10.1111/j.1600-048X.2012.00129.x
  • PLoS Biology
    2013

    The case of the missing mechanism: how does temperature influence seasonal timing in endotherms?

    Samuel P. Caro, Sonja Schaper, R.A. Hut, G.F. Ball, Marcel E. Visser
    Temperature has a strong effect on the seasonal timing of life-history stages in both mammals and birds, even though these species can regulate their body temperature under a wide range of ambient temperatures. Correlational studies showing this effect have recently been supported by experiments demonstrating a direct, causal relationship between ambient temperature and seasonal timing. Predicting how endotherms will respond to global warming requires an understanding of the physiological mechanisms by which temperature affects the seasonal timing of life histories. These mechanisms, however, remain obscure. We outline a road map for research aimed at identifying the pathways through which temperature is translated into seasonal timing.
    https://doi.org/10.1371/journal.pbio.1001517
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    2013

    Predicting demographically-sustainable rates of adaptation: can great tit breeding time keep pace with climate change?

    Phillip Gienapp, Marjolein Lof, Thomas Reed, J.M. McNamara, S. Verhulst, Marcel E. Visser
    Populations need to adapt to sustained climate change, which requires micro-evolutionary change in the long term. A key question is how the rate of this micro-evolutionary change compares with the rate of environmental change, given that theoretically there is a ‘critical rate of environmental change’ beyond which increased maladaptation leads to population extinction. Here, we parametrize two closely related models to predict this critical rate using data from a long-term study of great tits (Parus major). We used stochastic dynamic programming to predict changes in optimal breeding time under three different climate scenarios. Using these results we parametrized two theoretical models to predict critical rates. Results from both models agreed qualitatively in that even ‘mild’ rates of climate change would be close to these critical rates with respect to great tit breeding time, while for scenarios close to the upper limit of IPCC climate projections the calculated critical rates would be clearly exceeded with possible consequences for population persistence. We therefore tentatively conclude that micro-evolution, together with plasticity, would rescue only the population from mild rates of climate change, although the models make many simplifying assumptions that remain to be tested.
    https://doi.org/10.1098/rstb.2012.0289
  • Journal of Evolutionary Biology
    2013

    Genetic background, and not ontogenetic effects, affect avian seasonal timing of reproduction

    Phillip Gienapp, Arie Van Noordwijk, Marcel E. Visser
    Avian seasonal timing is a life-history trait with important fitness consequences and which is currently under directional selection due to climate change. To predict micro-evolution in this trait, it is crucial to properly estimate its heritability. Heritabilities are often estimated from pedigreed wild populations. As these are observational data, it leaves the possibility that the resemblance between related individuals is not due to shared genes but to ontogenetic effects; when the environment for the offspring provided by early laying pairs differs from that by late pairs and the laying dates of these offspring when they reproduce themselves is affected by this environment, this may lead to inflated heritability estimates. Using simulation studies, we first tested whether and how much such an early environmental effect can inflate heritability estimates from animal models, and we showed that pedigree structure determines by how much early environmental effects inflate heritability estimates. We then used data from a wild population of great tits (Parus major) to compare laying dates of females born early in the season in first broods and from sisters born much later, in second broods. These birds are raised under very different environmental conditions but have the same genetic background. The laying dates of first and second brood offspring do not differ when they reproduce themselves, clearly showing that ontogenetic effects are very small and hence, family resemblance in timing is due to genes. This finding is essential for the interpretation of the heritabilities reported from wild populations and for predicting micro-evolution in response to climate change.
    https://doi.org/10.1111/jeb.12205
  • Journal of Animal Ecology
    2013

    Phenological mismatch strongly affects individual fitness but not population demography in a woodland passerine

    Thomas Reed, S. Jenouvrier, Marcel E. Visser
    Populations are shifting their phenology in response to climate change, but these shifts are often asynchronous among interacting species. Resulting phenological mismatches can drive simultaneous changes in natural selection and population demography, but the links between these interacting processes are poorly understood. Here we analyse 37 years of data from an individual-based study of great tits (Parus major) in the Netherlands and use mixed-effects models to separate the within- and across-year effects of phenological mismatch between great tits and caterpillars (a key food source for developing nestlings) on components of fitness at the individual and population levels. Several components of individual fitness were affected by individual mismatch (i.e. late breeding relative to the caterpillar food peak date), including the probability of double-brooding, fledgling success, offspring recruitment probability and the number of recruits. Together these effects contributed to an overall negative relationship between relative fitness and laying dates, that is, selection for earlier laying on average. Directional selection for earlier laying was stronger in years where birds bred on average later than the food peak, but was weak or absent in years where the phenology of birds and caterpillars matched (i.e. no population mismatch). The mean number of fledglings per female was lower in years when population mismatch was high, in part because fewer second broods were produced. Population mismatch had a weak effect on the mean number of recruits per female, and no effect on mean adult survival, after controlling for the effects of breeding density and the quality of the autumnal beech (Fagus sylvatica) crop. These findings illustrate how climate change-induced mismatch can have strong effects on the relative fitness of phenotypes within years, but weak effects on mean demographic rates across years. We discuss various general mechanisms that influence the extent of coupling between breeding phenology, selection and population dynamics in open populations subject to strong density regulation and stochasticity.
    https://doi.org/10.1111/j.1365-2656.2012.02020.x
  • Ecology Letters
    2013

    Birds exploit herbivore-induced plant volatiles to locate herbivorous prey

    Luisa Amo de Paz, Jeroen Jansen, Nicole M. van Dam, Marcel Dicke, Marcel E. Visser
    Arthropod herbivory induces plant volatiles that can be used by natural enemies of the herbivores to find their prey. This has been studied mainly for arthropods that prey upon or parasitise herbivorous arthropods but rarely for insectivorous birds, one of the main groups of predators of herbivorous insects such as lepidopteran larvae. Here, we show that great tits (Parus major) discriminate between caterpillar-infested and uninfested trees. Birds were attracted to infested trees, even when they could not see the larvae or their feeding damage. We furthermore show that infested and uninfested trees differ in volatile emissions and visual characteristics. Finally, we show, for the first time, that birds smell which tree is infested with their prey based on differences in volatile profiles emitted by infested and uninfested trees. Volatiles emitted by plants in response to herbivory by lepidopteran larvae thus not only attract predatory insects but also vertebrate predators.
    https://doi.org/10.1111/ele.12177
  • Science Magazine
    2013

    Population growth in a wild bird is buffered against phenological mismatch

    Thomas Reed, V. Grotan, S. Jenouvrier, B-E. Sæther, Marcel E. Visser
    road-scale environmental changes are altering patterns of natural selection in the wild, but few empirical studies have quantified the demographic cost of sustained directional selection in response to these changes. We tested whether population growth in a wild bird is negatively affected by climate change–induced phenological mismatch, using almost four decades of individual-level life-history data from a great tit population. In this population, warmer springs have generated a mismatch between the annual breeding time and the seasonal food peak, intensifying directional selection for earlier laying dates. Interannual variation in population mismatch has not, however, affected population growth. We demonstrated a mechanism contributing to this uncoupling, whereby fitness losses associated with mismatch are counteracted by fitness gains due to relaxed competition. These findings imply that natural populations may be able to tolerate considerable maladaptation driven by shifting climatic conditions without undergoing immediate declines.
    https://doi.org/10.1126/science.1232870
  • Nature Climate Change
    2013

    Evolutionary response of the egg hatching date of a herbivorous insect under climate change

    M. Van Asch, Lucia Salis, L.J.M. Holleman, Bart van Lith, Marcel E. Visser
    Under changing climatic conditions, species need to adapt to their new environment. Genetic adaptation is crucial to prevent population extinction1 but examples where climate change leads to genetic changes in wild populations have been few2, 3. The synchronization between the timing of egg hatching of a herbivorous insect, the winter moth (Operophtera brumata), and the seasonal bud burst of its food plant, oak (Quercus robur), has been disrupted by climate change4 and a quantitative genetic model predicts that selection will delay the egg hatching date5. Here we show, using both long-term observational data and experiments, that the egg hatching date has changed genetically, resulting in closer synchrony with oak bud burst. The observed rate of change matches the predicted rate of change of one day per year. Hence, altered selection pressures, caused by environmental change, result in a rapid adaptive response in insect phenology. These genetic changes in a key life-history trait in this herbivorous insect therefore seem to be fast enough to match the climate-change-induced advancement of their host phenology.
    https://doi.org/10.1038/NCLIMATE1717
  • Journal of Evolutionary Biology
    2013

    Heritability of gonad size varies across season in a wild songbird

    Sonja Schaper, Phillip Gienapp, A. Dawson, Marcel E. Visser
    Many organisms advance their seasonal reproduction in response to global warming. In birds, which regress their gonads to a nonfunctional state each winter, these shifts are ultimately constrained by the time required for gonadal development in spring. Gonadal development is photoperiodically controlled and shows limited phenotypic plasticity in relation to environmental factors, such as temperature. Heritable variation in the time required for full gonadal maturation to be completed, based on both onset and speed of development and resulting in seasonally different gonad sizes among individuals, is thus a crucial prerequisite for an adaptive advancement of seasonal reproduction in response to changing temperatures. We measured seasonal gonadal development in climate-controlled aviaries for 144 great tit (Parus major) pairs, which consisted of siblings obtained as whole broods from the wild. We show that the extent of ovarian follicle development (follicle size) in early spring is highly heritable (h2 = 0.73) in females, but found no heritability of the extent of testis development in males. However, heritability in females decreased as spring advanced, caused by an increase in environmental variance and a decrease in additive genetic variation. This low heritability of the variation in a physiological mechanism underlying reproductive timing at the time of selection may hamper genetic adaptation to climate change, a key insight as this great tit population is currently under directional selection for advanced egg-laying.
    https://doi.org/10.1111/jeb.12249
  • General and Comparative Endocrinology
    2013

    Is microevolution the only emergency exit in a warming world? Temperature influences egg laying but not its underlying mechanisms in great tits

    Samuel P. Caro, Sonja Schaper, A. Dawson, P. Sharp, Phillip Gienapp, Marcel E. Visser
    Many bird species have advanced their seasonal timing in response to global warming, but we still know little about the causal effect of temperature. We carried out experiments in climate-controlled aviaries to investigate how temperature affects luteinizing hormone, prolactin, gonadal development, timing of egg laying and onset of moult in male and female great tits. We used both natural and artificial temperature patterns to identify the temperature characteristics that matter for birds. Our results show that temperature has a direct, causal effect on onset of egg-laying, and in particular, that it is the pattern of increase rather than the absolute temperature that birds use. Surprisingly, the pre-breeding increases in plasma LH, prolactin and in gonadal size are not affected by increasing temperature, nor do they correlate with the onset of laying. This suggests that the decision to start breeding and its regulatory mechanisms are fine-tuned by different factors. We also found similarities between siblings in the timing of both the onset of reproduction and associated changes in plasma LH, prolactin and gonadal development. In conclusion, while temperature affects the timing of egg laying, the neuroendocrine system does not seem to be regulated by moderate temperature changes. This lack of responsiveness may restrain the advance in the timing of breeding in response to climate change. But as there is heritable genetic variation on which natural selection can act, microevolution can take place, and may represent the only way to adapt to a warming world.
    https://doi.org/10.1016/j.ygcen.2013.02.025
  • Evolutionary Ecology
    2013

    Feather mass and winter moult extent are heritable but not associated with fitness-related traits in a long-distance migratory bird

    Iván De la Hera, Thomas Reed, F. Pulido, Marcel E. Visser
    In birds, the allocation of resources to plumage production may have important fitness consequences. However, we have only a limited understanding of how plumage traits respond to natural selection, making it difficult to predict how variation in plumage traits may contribute to the adaptation of birds to environmental change. In this study, we collected plumage-related data in a pedigreed population of a long-distance migratory bird (the Pied Flycatcher Ficedula hypoleuca) to estimate the heritability of two plumage traits: feather mass (as a proxy of feather quality) and the extent of winter moult. We further explored whether these plumage features were associated with some fitness-related traits. Variation in plumage characteristics could be explained by differences in sex, age and year, which indicates a high degree of plasticity in these traits. After controlling for these effects, however, feather mass and winter moult extent were highly repeatable (r = 0.58–0.82) and heritable (h2 = 0.59–0.65), suggesting that additive genetic variation accounts for a significant proportion of the residual phenotypic variation of plumage traits in this population. Although the studied characteristics showed evolutionary potential, we did not find any relationship between plumage features and fitness-related traits like spring arrival date, egg-laying date, mating success or mating-time. We conclude that current selection on feather mass and moult extent, if existing, is weak, and that these moult-related traits are currently of minor importance for the adaptation of our study population to global warming.
    https://doi.org/10.1007/s10682-013-9639-x
  • Journal of Ornithology
    2012

    Adaptive phenological mismatches of birds and their food in a warming world

    Marcel E. Visser, Luc te Marvelde, Marjolein Lof
    Climate change has profound ecological effects in birds, with the clearest effect a shift in timing, or phenology, of avian reproduction. To assess the consequences of these shifts, we performed a literature search and compared the rates of phenological change in the reproduction of birds with that of the food for their offspring. While in some areas the rate of change of the birds and their food was similar, there were also areas where the birds’ shift lagged behind that of their food. In these cases, this will lead to a phenological mismatch, which will affect the fitness of the brood. There are two hypotheses explaining why climate change leads to mismatched reproduction: either the cues used no longer accurately predict the peak in food abundance (the cues hypothesis) or the fitness costs of egg production and/or incubation of laying early enough to match reproduction are substantial in early spring and are not compensated by the fitness benefits of a better matched reproduction (constraint hypothesis). In the latter case, the phenological mismatch is adaptive. We present a simple mathematical model to show that this may be the case if there are fitness costs of egg laying and/or incubation under cold conditions and if the temperatures that determine the peak in food abundance increase stronger than the temperatures affecting the costs of egg laying and incubation, as is the case in the Netherlands. Whether or not a phenological mismatch is adaptive has important consequences for natural selection acting on timing of reproduction. If the mismatch is not adaptive, timing of reproduction will be under direct natural selection, while, if the mismatch is adaptive, selection is likely to be on the costs of egg production, possibly on egg size or adult size. In all cases, a mismatch is expected to have negative population consequences and, especially when the mismatch is adaptive, these consequences cannot be reduced by a response to natural selection on timing directly. This makes experimental studies on laying date, which can determine whether the mismatch is adaptive, of crucial importance.
    https://doi.org/10.1007/s10336-011-0770-6
  • Proceedings of the Royal Society B-Biological Sciences
    2012

    Timing in a fluctuating environment: environmental variability and asymmetric fitness curves can lead to adaptively mismatched avian reproduction

    Marjolein Lof, Thomas Reed, J.M. McNamara, Marcel E. Visser
    Adaptation in dynamic environments depends on the grain, magnitude and predictability of ecological fluctuations experienced within and across generations. Phenotypic plasticity is a well-studied mechanism in this regard, yet the potentially complex effects of stochastic environmental variation on optimal mean trait values are often overlooked. Using an optimality model inspired by timing of reproduction in great tits, we show that temporal variation affects not only optimal reaction norm slope, but also elevation. With increased environmental variation and an asymmetric relationship between fitness and breeding date, optimal timing shifts away from the side of the fitness curve with the steepest decline. In a relatively constant environment, the timing of the birds is matched with the seasonal food peak, but they become adaptively mismatched in environments with temporal variation in temperature whenever the fitness curve is asymmetric. Various processes affecting the survival of offspring and parents influence this asymmetry, which collectively determine the ‘safest’ strategy, i.e. whether females should breed before, on, or after the food peak in a variable environment. As climate change might affect the (co)variance of environmental variables as well as their averages, risk aversion may influence how species should shift their seasonal timing in a warming world.
    https://doi.org/10.1098/rspb.2012.0431
  • General and Comparative Endocrinology
    2012

    Individual variation in avian reproductive physiology does not reliably predict variation in laying date

    Sonja Schaper, A. Dawson, P.J. Sharp, Samuel P. Caro, Marcel E. Visser
    Most animals reproduce seasonally. They time their reproduction in response to environmental cues, like increasing photoperiod and temperature, which are predictive for the time of high food availability. Although individuals of a population use the same cues, they vary in their onset of reproduction, with some animals reproducing consistently early or late. In avian research, timing of reproduction often refers to the laying date of the first egg, which is a key determinant of fitness. Experiments measuring temporal patterns of reproductive hormone concentrations or gonadal size under controlled conditions in response to a cue commonly assume that these proxies are indicative of the timing of egg laying. This assumption often remains untested, with few studies reporting both reproductive development and the onset of laying. We kept in total 144 pairs of great tits (Parus major) in separate climate-controlled aviaries over 4 years to correlate pre-breeding plasma luteinizing hormone (LH), prolactin (PRL) and gonadal growth with the timing of laying. Individuals varied consistently in hormone concentrations over spring, but this was not directly related to the timing of gonadal growth, nor with the laying date of the first egg. The timing of gonadal development in both sexes was similarly not correlated with the timing of laying. This demonstrates the female’s ability to adjust the onset of laying to environmental conditions irrespective of substantial differences in pre-laying development. We conclude that stages of reproductive development are regulated by different cues, and therefore egg laying dates need to be studied to measure the influences of environmental cues on timing of seasonal reproduction.
    https://doi.org/10.1016/j.ygcen.2012.07.021
  • Oecologia
    2012

    Energy expenditure during egg laying is equal for early and late breeding free-living female great tits

    Luc te Marvelde, S.L. Webber, H.A.J. Meijer, Marcel E. Visser
    In many bird populations, variation in the timing of reproduction exists but it is not obvious how this variation is maintained as timing has substantial fitness consequences. Daily energy expenditure (DEE) during the egg laying period increases with decreasing temperatures and thus perhaps only females that can produce eggs at low energetic cost will lay early in the season, at low temperatures. We tested whether late laying females have a higher daily energy expenditure during egg laying than early laying females in 43 great tits (Parus major), by comparing on the same day the DEE of early females late in their laying sequence with DEE of late females early in their egg laying sequence. We also validated the assumption that there are no within female differences in DEE within the egg laying sequence. We found a negative effect of temperature and a positive effect of female body mass on DEE but no evidence for differences in DEE between early and late laying females. However, costs incurred during egg laying may have carry-over effects later in the breeding cycle and if such carry-over effects differ for early and late laying females this could contribute to the maintenance of phenotypic variation in laying dates.
    https://doi.org/10.1007/s00442-011-2122-x
  • American Naturalist
    2012

    Increasing temperature, not mean temperature, is a cue for avian timing of reproduction

    Sonja Schaper, A. Dawson, P. Sharp, Phillip Gienapp, Samuel P. Caro, Marcel E. Visser
    Timing of reproduction in temperate-zone birds is strongly correlated with spring temperature, with an earlier onset of breeding in warmer years. Females adjust their timing of egg laying between years to be synchronized with local food sources and thereby optimize reproductive output. However, climate change currently disrupts the link between predictive environmental cues and spring phenology. To investigate direct effects of temperature on the decision to lay and its genetic basis, we used pairs of great tits (Parus major) with known ancestry and exposed them to simulated spring scenarios in climate-controlled aviaries. In each of three years, we exposed birds to different patterns of changing temperature. We varied the timing of a temperature change, the daily temperature amplitude, and the onset and speed of a seasonal temperature rise. We show that females fine-tune their laying in response to a seasonal increase in temperature, whereas mean temperature and daily temperature variation alone do not affect laying dates. Luteinizing hormone concentrations and gonadal growth in early spring were not influenced by temperature or temperature rise, possibly posing a constraint to an advancement of breeding. Similarities between sisters in their laying dates indicate genetic variation in cue sensitivity. These results refine our understanding of how changes in spring climate might affect the mismatch in avian timing and thereby population viability.
    https://doi.org/10.1086/663675
  • Journal of Animal Ecology
    2012

    Climate change, breeding date and nestling diet: how temperature differentially affects seasonal changes in pied flycatcher diet depending on habitat variation

    C. Burger, E. Belskii, T. Eeva, T. Laaksonen, M. Mägi, R. Mänd, A. Qvarnström, T. Slagsvold, T. Veen, Marcel E. Visser, K.L. Wiebe, C. Wiley, J. Wright, Christiaan Both
    1.Climate warming has led to shifts in the seasonal timing of species. These shifts can differ across trophic levels, and as a result, predator phenology can get out of synchrony with prey phenology. This can have major consequences for predators such as population declines owing to low reproductive success. However, such trophic interactions are likely to differ between habitats, resulting in differential susceptibility of populations to increases in spring temperatures. A mismatch between breeding phenology and food abundance might be mitigated by dietary changes, but few studies have investigated this phenomenon. Here, we present data on nestling diets of nine different populations of pied flycatchers Ficedula hypoleuca, across their breeding range. This species has been shown to adjust its breeding phenology to local climate change, but sometimes insufficiently relative to the phenology of their presumed major prey: Lepidoptera larvae. In spring, such larvae have a pronounced peak in oak habitats, but to a much lesser extent in coniferous and other deciduous habitats. 2.We found strong seasonal declines in the proportions of caterpillars in the diet only for oak habitats, and not for the other forest types. The seasonal decline in oak habitats was most strongly observed in warmer years, indicating that potential mismatches were stronger in warmer years. However, in coniferous and other habitats, no such effect of spring temperature was found. 3.Chicks reached somewhat higher weights in broods provided with higher proportions of caterpillars, supporting the notion that caterpillars are an important food source and that the temporal match with the caterpillar peak may represent an important component of reproductive success. 4.We suggest that pied flycatchers breeding in oak habitats have greater need to adjust timing of breeding to rising spring temperatures, because of the strong seasonality in their food. Such between-habitat differences can have important consequences for population dynamics and should be taken into account in studies on phenotypic plasticity and adaptation to climate change.
    https://doi.org/10.1111/j.1365-2656.2012.01968.x
  • Molecular Ecology Resources
    2012

    The design and cross-population application of a genome-wide SNP chip for the great tit Parus major

    N.E.M. Van Bers, A.W. Santure, Kees van Oers, I. de Cauwer, B.W. Dibbits, A.C. Mateman, R.P.M.A. Crooijmans, Ben C. Sheldon, Marcel E. Visser, M.A.M. Groenen, J. Slate
    The vast amount of phenotypic information collected in some wild animal populations makes them extremely valuable for unravelling the genetics of ecologically important traits and understanding how populations adapt to changes in their environment. Next generation sequencing has revolutionized the development of large marker panels in species previously lacking genomic resources. In this study, a unique genomics toolkit was developed for the great tit (Parus major), a model species in ecology and behavioural biology. This toolkit consists of nearly 100 000 SNPs, over 250 million nucleotides of assembled genomic DNA and more than 80 million nucleotides of assembled expressed sequences. A SNP chip with 9193 SNP markers expected to be spaced evenly along the great tit genome was used to genotype 4702 birds from two of the most intensively studied natural vertebrate populations [Wytham Woods/Bagley Woods (United Kingdom) and de Hoge Veluwe/Westerheide (The Netherlands)]. We show that (i) SNPs identified in either of the two populations have a high genotyping success in the other population, (ii) the minor allele frequencies of the SNPs are highly correlated between the two populations and (iii) despite this high correlation, a large number of SNPs display significant differentiation (FST) between the populations, with an overrepresentation of genes involved in cardiovascular development close to these SNPs. The developed resources provide the basis for unravelling the genetics of important traits in many long-term studies of great tits. More generally, the protocols and pitfalls encountered will be of use for those developing similar resources.
    https://doi.org/10.1111/j.1755-0998.2012.03141.x
  • Nature Climate Change
    2012

    Biology: Birds and butterflies in climatic debt

    A European-wide analysis of changing species distributions shows that butterflies outrun birds in the race to move northwards in response to climate change, but that neither group keeps up with increasing temperatures.
    https://doi.org/10.1038/nclimate1387
  • PLoS One
    2012

    A single long day triggers follicle growth in captive female Great Tits (Parus major) in winter but does not affect laying dates in the wild in spring

    Luc te Marvelde, Sonja Schaper, Marcel E. Visser
    In many forest passerine bird species, rapid climate warming has led to a phenological mismatch between the period of maximum nestlings' food requirements and the period of maximum food availability (seasonal caterpillar biomass peak) due to an insufficient advancement of the birds' laying dates. The initiation of laying is preceded by the development of the gonads, which in birds are regressed outside the breeding season. Increasing day length in late winter and early spring triggers a cascade of hormones which induces gonadal development. Since day length is not altered by climate change, one potential restriction to advancing laying date is the seasonal timing of gonadal development. To assess the importance of gonadal growth for timing of reproduction we experimentally manipulated the timing of gonadal development. We show that the growth of the largest follicle of captive female great tits (Parus major) increased after being exposed to just a single long day in winter (20 hours of light followed by 4 hours darkness). We then photostimulated wild female great tits from two study areas in a field experiment in spring for a single day and determined their laying date. These populations differed in the availability of food allowing us to test if food availability in combination with photostimulation affected egg laying dates. Despite an expected difference in the onset of gonadal growth, laying dates of photostimulated females did not differ from control females in both populations. These results suggest that wild great tits are not restricted in the advancement of their laying date by limited gonadal development.
    https://doi.org/10.1371/journal.pone.0035617
  • PLoS One
    2012

    Activity patterns during food provisioning are affected by artificial light in free living great tits (Parus major)

    Mieke Titulaer, Kamiel Spoelstra, Cynthia Lange, Marcel E. Visser
    Artificial light may have severe ecological consequences but there is limited experimental work to assess these consequences. We carried out an experimental study on a wild population of great tits (Parus major) to assess the impact of light pollution on daily activity patterns during the chick provisioning period. Pairs that were provided with a small light outside their nest box did not alter the onset, cessation or duration of their working day. There was however a clear effect of artificial light on the feeding rate in the second half of the nestling period: when provided with artificial light females increased their feeding rate when the nestlings were between 9 and 16 days old. Artificial light is hypothesised to have affected the perceived photoperiod of either the parents or the offspring which in turn led to increased parental care. This may have negative fitness consequences for the parents, and light pollution may thus create an ecological trap for breeding birds.
    https://doi.org/10.1371/journal.pone.0037377
  • Annual Review of Chronopharmacology
    2012

    Effects of temperature on circadian clock and chronotype: an experimental study in a passerine bird

    M. Lehmann, Kamiel Spoelstra, Marcel E. Visser, B. Helm
    Daily schedules of many organisms, including birds, are thought to affect fitness. Timing in birds is based on circadian clocks that have a heritable period length, but fitness consequences for individuals in natural environments depend on the scheduling of entrained clocks. This chronotype, i.e., timing of an individual relative to a zeitgeber, results from interactions between the endogenous circadian clock and environmental factors, including light conditions and ambient temperature. To understand contributions of these factors to timing, we studied daily activity patterns of a captive songbird, the great tit (Parus major), under different temperature and light conditions. Birds were kept in a light (L)-dark (D) cycle (12.5 L:11.5 D) at either 8°C or 18°C with ad libitum access to food and water. We assessed chronotype and subsequently tested birds at the same temperature under constant dim light (LLdim) to determine period length of their circadian clock. Thermal conditions were then reversed so that period length was measured under both temperatures. We found that under constant dim light conditions individuals lengthened their free-running period at higher temperatures by 5.7 ± 2.1 min (p = .002). Under LD, birds kept at 18°C started activity later and terminated it much earlier in the day than those kept under 8°C. Overall, chronotype was slightly earlier under higher temperature, and duration of activity was shorter. Furthermore, individuals timed their activities consistently on different days under LD and over the two test series under LLdim (repeatability from .38 to .60). Surprisingly, period length and chronotype did not show the correlation that had been previously found in other avian species. Our study shows that body clocks of birds are precise and repeatable, but are, nonetheless, affected by ambient temperature.
    https://doi.org/10.3109/07420528.2012.707159
  • PLoS One
    2012

    Manipulation of life-history decisions using leptin in a wild passerine

    Luc te Marvelde, Marcel E. Visser
    Seasonal timing of reproduction and the number of clutches produced per season are two key avian life-history traits with major fitness consequences. Female condition may play an important role in these decisions. In mammals, body condition and leptin levels are correlated. In birds, the role of leptin remains unclear. We did two experiments where we implanted female great tits with a pellet releasing leptin evenly for 14 days, to manipulate their perceived body condition, or a placebo pellet. In the first experiment where females were implanted when feeding their first brood offspring we found, surprisingly, that placebo treated females were more likely to initiate a second brood compared to leptin treated females. Only one second brood fledged two chicks while five were deserted late in the incubation stage or when the first egg hatched. No difference was found in female or male return rate or in recruitment rate of fledglings of the first brood, possibly due to the desertion of the second broods. In our study population, where there is selection for early egg laying, earlier timing of reproduction might be hampered by food availability and thus nutritional state of the female before egg laying. We therefore implanted similar leptin pellets three weeks before the expected start of egg laying in an attempt to manipulate the laying dates of first clutches. However, leptin treated females did not initiate egg laying earlier compared to placebo treated females, suggesting that other variables than the perceived body condition play a major role in the timing of reproduction. Also, leptin treatment did not affect body mass, basal metabolic rate or feeding rates in captive females. Manipulating life history decisions using experimental protocols which do not alter individuals’ energy balance are crucial in understanding the trade-off between costs and benefits of life history decisions.
    https://doi.org/10.1371/journal.pone.0034090
  • Functional Ecology
    2011

    Genetic variation in cue sensitivity involved in avian timing of reproduction

    Marcel E. Visser, Sonja Schaper, L.J.M. Holleman, A. Dawson, P. Sharp, Phillip Gienapp, Samuel P. Caro
    1.Annual variation in the timing of avian reproduction is associated with predictive cues related to ambient temperature. Understanding how these cues affect timing, and estimating the genetic variation in sensitivity to these cues, is essential to predict the micro-evolutionary changes in timing which are needed to adapt to climate change. 2.We carried out a 2-year experiment with great tits Parus major of known genetic background, which were kept in pairs in climate-controlled aviaries with simulated natural photoperiod and exposed to a seasonal change in temperature, where the two treatments differed by 4 °C. We recorded the dates of laying the first and last eggs and timing of moult, as well as physiological proxies associated with reproduction: plasma luteinizing hormone (LH), prolactin, and gonadal size at four-weekly intervals. 3.The temperature treatments did not affect first-egg dates, nor gonadal growth or plasma LH and prolactin concentrations. However, birds terminated egg laying, regressed their testes and started their moult earlier at higher temperatures. 4.There were marked family differences in both the start of egg laying, with sisters from early laying maternal families laying early, and in the termination of laying, indicating that there is heritable variation in sensitivity to cues involved in timing. 5.Our experiment, the first to use genetically related individuals in an experimental design with a natural change in photoperiod and biologically realistic temperature differences, thus shows that genetic adaptation in cue sensitivity is possible, essential for species to be able to adapt to a warming world.
    https://doi.org/10.1111/j.1365-2435.2011.01844.x
  • Ardea
    2011

    Smelling out predators is innate in birds

    Luisa Amo de Paz, Marcel E. Visser, Kees van Oers
    The role of olfaction for predation risk assessment remains barely explored in birds, although predator chemical cues could be useful in predator detection under low visibility conditions for many bird species. We examine whether Great Tits Parus major are able to use the odour of mustelids to assess predation risk when selecting cavities for roosting. We analysed whether the response to predator chemical cues is innate and assessed whether the antipredatory response is associated with exploratory behaviour, a proxy for the personality of birds. In a choice experiment in aviaries, we offered naïve adult Great Tits of known personality two nest-boxes, one control and one experimental. The experimental nest-box had the odour of a mustelid predator or a strong new odour without biological significance, the control nest-box contained no odour. When one of the cavities contained the odour of a predator, birds avoided the use of either of the two offered nest-boxes, whereas there was no avoidance of boxes when one of the nest-boxes contained a control odour. There was no relationship with exploratory behaviour. We show that the ability to use the chemical cues of predators is innate in birds, but individual differences in the response to predator chemical cues cannot be explained by the personality of the bird.
    https://doi.org/10.5253/078.099.0207
  • Journal of Experimental Biology
    2011

    Spring phenology does not affect timing of reproduction in the great tit (Parus major)

    Sonja Schaper, C. Rueda, P.J. Sharp, A. Dawson, Marcel E. Visser
    Many seasonal breeders adjust the timing of reproduction in response to year-to-year variations in supplementary environmental cues, amongst which ambient temperature is thought to be most influential. However, it is possible that for species such as the great tit (Parus major L.), phenological cues from sprouting vegetation and the consequent abundance of invertebrate prey, although dependent on temperature, may provide supplementary environmental cues per se. This hypothesis was investigated in breeding pairs of great tits kept in outdoor aviaries. In spring, experimental pairs were provided with access to leafing birch branches and caterpillars as a visual food cue, while control pairs were provided with non-leafing branches. Observations were made on the onset of laying and on concentrations of plasma luteinizing hormone (LH) at regular intervals to monitor changes in reproductive function. The onset of egg laying was not advanced by the presence of leafing branches and caterpillars. LH concentrations increased during the course of the study, but phenological cues did not affect plasma LH levels in females and males. Early spring vegetation, such as the leafing of birch branches, and the appearance of caterpillar prey do not appear to play a significant role in fine-tuning the onset of egg laying in great tits.
    https://doi.org/10.1242/jeb.059543
  • PLoS One
    2011

    Geographical variation in egg mass and egg content in a passerine bird

    Suvi Ruuskanen, H. Siitari, T. Eeva, E. Belskii, A. Järvinen, A. Kerimov, I. Krams, J. Moreno, C. Morosinotto, R. Mänd, E. Möstl, M. Orell, A. Qvarnström, J.P. Salminen, F.M. Slater, V. Tilgar, Marcel E. Visser, W. Winkel, H. Zang, T. Laaksonen
    Reproductive, phenotypic and life-history traits in many animal and plant taxa show geographic variation, indicating spatial variation in selection regimes. Maternal deposition to avian eggs, such as hormones, antibodies and antioxidants, critically affect development of the offspring, with long-lasting effects on the phenotype and fitness. Little is however known about large-scale geographical patterns of variation in maternal deposition to eggs. We studied geographical variation in egg components of a passerine bird, the pied flycatcher (Ficedula hypoleuca), by collecting samples from 16 populations and measuring egg and yolk mass, albumen lysozyme activity, yolk immunoglobulins, yolk androgens and yolk total carotenoids. We found significant variation among populations in most egg components, but ca. 90% of the variation was among individuals within populations. Population however explained 40% of the variation in carotenoid levels. In contrast to our hypothesis, we found geographical trends only in carotenoids, but not in any of the other egg components. Our results thus suggest high within-population variation and leave little scope for local adaptation and genetic differentiation in deposition of different egg components. The role of these maternally-derived resources in evolutionary change should be further investigated.
    https://doi.org/10.1371/journal.pone.0025360
  • American Naturalist
    2011

    Testing mechanisms of Bergmann’s rule: Phenotypic decline but no genetic change in body size in three posserine bird populations

    A. Husby, S.M. Hille, Marcel E. Visser
    Bergmann’s rule predicts a decrease in body size with increasing temperature and has much empirical support. Surprisingly, we know very little about whether “Bergmann size clines” are due to a genetic response or are a consequence of phenotypic plasticity. Here, we use data on body size (mass and tarsus length) from three long-term (1979–2008) study populations of great tits (Parus major) that experienced a temperature increase to examine mechanisms behind Bergmann’s rule. We show that adult body mass decreased over the study period in all populations and that tarsus length increased in one population. Both body mass and tarsus length were heritable and under weak positive directional selection, predicting an increase, rather than a decrease, in body mass. There was no support for microevolutionary change, and thus the observed declines in body mass were likely a result of phenotypic plasticity. Interestingly, this plasticity was not in direct response to temperature changes but seemed to be due to changes in prey dynamics. Our results caution against interpreting recent phenotypic body size declines as adaptive evolutionary responses to temperature changes and highlight the importance of considering alternative environmental factors when testing size clines.
    https://doi.org/10.1086/660834
  • PLoS Biology
    2011

    Speeding up microevolution: the effects of increasing temperature on selection and genetic variance in a wild bird population

    A. Husby, Marcel E. Visser, L.E.B. Kruuk
    The amount of genetic variance underlying a phenotypic trait and the strength of selection acting on that trait are two key parameters that determine any evolutionary response to selection. Despite substantial evidence that, in natural populations, both parameters may vary across environmental conditions, very little is known about the extent to which they may covary in response to environmental heterogeneity. Here we show that, in a wild population of great tits (Parus major), the strength of the directional selection gradients on timing of breeding increased with increasing spring temperatures, and that genotype-by-environment interactions also predicted an increase in additive genetic variance, and heritability, of timing of breeding with increasing spring temperature. Consequently, we therefore tested for an association between the annual selection gradients and levels of additive genetic variance expressed each year; this association was positive, but non-significant. However, there was a significant positive association between the annual selection differentials and the corresponding heritability. Such associations could potentially speed up the rate of micro-evolution and offer a largely ignored mechanism by which natural populations may adapt to environmental changes.
    https://doi.org/10.1371/journal.pbio.1000585
  • PLoS One
    2011

    Sleeping birds do not respond to predator odour

    Luisa Amo de Paz, Samuel P. Caro, Marcel E. Visser
    Background: During sleep animals are relatively unresponsive and unaware of their environment, and therefore, more exposed to predation risk than alert and awake animals. This vulnerability might influence when, where and how animals sleep depending on the risk of predation perceived before going to sleep. Less clear is whether animals remain sensitive to predation cues when already asleep. Methodology/Principal Findings: We experimentally tested whether great tits are able to detect the chemical cues of a common nocturnal predator while sleeping. We predicted that birds exposed to the scent of a mammalian predator (mustelid) twice during the night would not go into torpor (which reduces their vigilance) and hence would not reduce their body temperature as much as control birds, exposed to the scent of another mammal that does not represent a danger for the birds (rabbit). As a consequence of the higher body temperature birds exposed to the scent of a predator are predicted to have a higher resting metabolic rate (RMR) and to lose more body mass. In the experiment, all birds decreased their body temperature during the night, but we did not find any influence of the treatment on body temperature, RMR, or body mass. Conclusions/Significance: Our results suggest that birds are not able to detect predator chemical cues while sleeping. As a consequence, antipredatory strategies taken before sleep, such as roosting sites inspection, may be crucial to cope with the vulnerability to predation risk while sleeping.
    https://doi.org/10.1371/journal.pone.0027576
  • Journal of Field Ornithology
    2011

    A new method for catching cavity-nesting birds during egg laying and incubation

    Luc te Marvelde, S.L. Webber, AB. Van den Burg, Marcel E. Visser
    The physiological condition of female birds during the egg-laying and incubation periods is of considerable interest and yet is relatively understudied in wild birds, primarily due to the difficulty of catching birds during this period without causing nest desertion. We therefore developed a box-net to capture cavity-nesting birds using sections of a mist-net placed around a metal cubic frame. We captured female Great Tits (Parus major) as they left nest boxes during the egg-laying and incubation periods and measured desertion rates. Using box-nets, we captured 108 of 119 (90%) females during egg laying and 10 of 12 (83%) during incubation. Our recapture rate over two consecutive days during incubation was 50% (5 of 10). Females not captured left nest boxes before we attempted to capture them, escaped through a hole in the mist-net, or remained in nest boxes for more than 2 h, after which we ended capture attempts. Overall, 22% of egg-laying females deserted, with desertion rates highest early in the egg-laying period. Desertion rates of females captured using box-nets did not differ from those of undisturbed females. One of 10 females captured in a box-net deserted during the incubation period. Box-nets are portable, can be set up and taken down quickly and easily, and could potentially be used with nest boxes or natural cavities at any height. Box-nets are easy to construct and adaptable for use with an array of cavity-nesting birds, and can be an important tool for studying female physiology during egg laying and incubation.
    https://doi.org/10.1111/j.1557-9263.2011.00335.x
  • International Journal of Biometeorology
    2011

    Climate change, phenological shifts, eco-evolutionary responses and population viability: toward a unifying predictive approach

    S. Jenouvrier, Marcel E. Visser
    The debate on emission targets of greenhouse gasses designed to limit global climate change has to take into account the ecological consequences. One of the clearest ecological consequences is shifts in phenology. Linking these shifts to changes in population viability under various greenhouse gasses emission scenarios requires a unifying framework. We propose a box-in-a-box modeling approach that couples population models to phenological change. This approach unifies population modeling with both ecological responses to climate change as well as evolutionary processes. We advocate a mechanistic embedded correlative approach, where the link from genes to population is established using a periodic matrix population model. This periodic model has several major advantages: (1) it can include complex seasonal behaviors allowing an easy link with phenological shifts; (2) it provides the structure of the population at each phase, including the distribution of genotypes and phenotypes, allowing a link with evolutionary processes; and (3) it can incorporate the effect of climate at different time periods. We believe that the way climatologists have approached the problem, using atmosphere–ocean coupled circulation models in which components are gradually included and linked to each other, can provide a valuable example to ecologists. We hope that ecologists will take up this challenge and that our preliminary modeling framework will stimulate research toward a unifying predictive model of the ecological consequences of climate change.
    https://doi.org/10.1007/s00484-011-0458-x
  • Journal of Insect Conservation
    2011

    Synchronisation of egg hatching of brown hairstreak (Thecla betulae) and budburst of blackthorn (Prunus spinosa) in a warmer future

    H.H. De Vries, S.H. Ens, G. de Graaf, L. Teunissen, R. te Velde, L. Vogelaar, A. Winterink, Marcel E. Visser
    Synchronisation of the phenology of insect herbivores and their larval food plant is essential for the herbivores’ fitness. The monophagous brown hairstreak (Thecla betulae) lays its eggs during summer, hibernates as an egg, and hatches in April or May in the Netherlands. Its main larval food plant blackthorn (Prunus spinosa) flowers in early spring, just before the leaves appear. As soon as the Blackthorn opens its buds, and this varies with spring temperatures, food becomes available for the brown hairstreak. However, the suitability of the leaves as food for the young caterpillars is expected to decrease rapidly. Therefore, the timing of egg hatch is an important factor for larval growth. This study evaluates food availability for brown hairstreak at different temperatures. Egg hatch and budburst were monitored from 2004 to 2008 at different sites in the Netherlands. Results showed ample food availability at all monitored temperatures and sites but the degree of synchrony varied strongly with spring temperatures. To further study the effect of temperature on synchronisation, an experiment using normal temperatures of a reference year (T) and temperatures of T + 5°C was carried out in climate chambers. At T + 5°C, both budburst and egg hatch took place about 20 days earlier and thus, on average, elevated temperature did not affect synchrony. However, the total period of budburst was 11 days longer, whereas the period of egg hatching was 3 days shorter. The implications for larval growth by the brown hairstreak under a warmer climate are considered.
    https://doi.org/10.1007/s10841-010-9355-6
  • Functional Ecology
    2011

    Mismatched reproduction is energetically costly for chick feeding female great tits

    Luc te Marvelde, S.L. Webber, H.A.J. Meijer, Marcel E. Visser
    1. Climate change has caused a phenological mismatch between the timing of reproduction and the local food peak in many bird species. Late breeding birds therefore experience reduced food availability during chick rearing and are thus predicted to have an increased energy expenditure. Observational studies, however, show mixed results, perhaps because they compare energy expenditure across rather than within individuals at different levels of food availability. 2. In a cross foster experiment, we measured daily energy expenditure (DEE) twice within individuals during chick feeding (when chicks were 6 and 14 days old) for 28 free-living female great tits (Parus major). To avoid confounding effects of chick age, these females reared on both occasions a standardized foster brood of eight 10-day-old chicks during the 24-h measuring period. For all birds, food availability declined between the two measurements. 3. We show that DEE during chick feeding increased within females when food availability decreased. Variation in DEE within females is partly explained by brood visit rates, food availability and temperature. 4. DEE during chick feeding could be affected by the investment in previous stages of the reproductive attempt. However, energy expenditure during chick feeding was not correlated to energy expenditure during egg laying, measured in these same females. 5. Understanding of energetic costs during all phases of the reproductive cycle is important to forecast the consequences of climate warming on timing of reproduction.
    https://doi.org/10.1111/j.1365-2435.2011.01889.x
  • Oecologia
    2011

    Geographical trends in the yolk carotenoid composition of the pied flycatcher (Ficedula hypoleuca)

    T. Eeva, Suvi Ruuskanen, J.P. Salminen, E. Belskii, A. Jarvinen, A. Kerimov, E. Korpimäki, I. Krams, J. Moreno, C. Morosinotto, R. Mänd, M. Orell, A. Qvarnström, H. Siitari, F.M. Slater, V. Tilgar, Marcel E. Visser, W. Winkel, H. Zang, T. Laaksonen
    Carotenoids in the egg yolks of birds are considered to be important antioxidants and immune stimulants during the rapid growth of embryos. Yolk carotenoid composition is strongly affected by the carotenoid composition of the female’s diet at the time of egg formation. Spatial and temporal differences in carotenoid availability may thus be reflected in yolk concentrations. To assess whether yolk carotenoid concentrations or carotenoid profiles show any large-scale geographical trends or differences among habitats, we collected yolk samples from 16 European populations of the pied flycatcher, Ficedula hypoleuca.Wefound that the concentrations and proportions of lutein and some other xanthophylls in the egg yolks decreased from Central Europe northwards. The most southern population (which is also the one found at the highest altitude) also showed relatively low carotenoid levels. Concentrations of b-carotene and zeaxanthin did not show any obvious geographical gradients. Egg yolks also contained proportionally more lutein and other xanthophylls in deciduous than in mixed or coniferous habitats. We suggest that latitudinal gradients in lutein and xanthophylls reflect the lower availability of lutein-rich food items in the northern F. hypoleuca populations and in montane southern populations, which start egg-laying earlier relative to tree phenology than the Central European populations. Similarly, among-habitat variation is likely to reflect the better availability of lutein-rich food in deciduous forests. Our study is the first to indicate that the concentration and profile of yolk carotenoids may show large-scale spatial variation among populations in different parts of the species’ geographical range. Further studies are needed to test the fitness effects of this geographical variation.
    https://doi.org/10.1007/s00442-010-1772-4
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    2010

    Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels

    Wim H. van der Putten, Mirka Macel, Marcel E. Visser
    Current predictions on species responses to climate change strongly rely on projecting altered environmental conditions on species distributions. However, it is increasingly acknowledged that climate change also influences species interactions. We review and synthesize literature information on biotic interactions and use it to argue that the abundance of species and the direction of selection during climate change vary depending on how their trophic interactions become disrupted. Plant abundance can be controlled by aboveground and belowground multitrophic level interactions with herbivores, pathogens, symbionts and their enemies. We discuss how these interactions may alter during climate change and the resulting species range shifts. We suggest conceptual analogies between species responses to climate warming and exotic species introduced in new ranges. There are also important differences: the herbivores, pathogens and mutualistic symbionts of range-expanding species and their enemies may co-migrate, and the continuous gene flow under climate warming can make adaptation in the expansion zone of range expanders different from that of cross-continental exotic species. We conclude that under climate change, results of altered species interactions may vary, ranging from species becoming rare to disproportionately abundant. Taking these possibilities into account will provide a new perspective on predicting species distribution under climate change.
    https://doi.org/10.1098/rstb.2010.0037
  • Proceedings of the Royal Society B-Biological Sciences
    2010

    Heritable circadian period length in a wild bird population

    B. Helm, Marcel E. Visser
    Timing is essential, but circadian clocks, which play a crucial role in timekeeping, are almost unaddressed in evolutionary ecology. A key property of circadian clocks is their free-running period length (τ), i.e. the time taken for a full cycle under constant conditions. Under laboratory conditions, concordance of τ with the ambient light–dark cycle confers major fitness benefits, but little is known about period length and its implications in natural populations. We therefore studied natural variation of circadian traits in a songbird, the great tit (Parus major), by recording locomotor activity of 98 hand-raised, wild-derived individuals. We found, unexpectedly, that the free-running period of this diurnal species was significantly shorter than 24 h in constant dim light. We furthermore demonstrate, to our knowledge for the first time in a wild vertebrate, ample genetic variation and high heritability (h2 = 0.86 ± 0.24), implying that period length is potentially malleable by micro-evolutionary change. The observed, short period length may be a consequence of sexual selection, as offspring from extra-pair matings had significantly shorter free-running periods than their half-siblings from within-pair matings. These findings position circadian clocks in the ‘real world’ and underscore the value of using chronobiological approaches in evolutionary ecology. Evolutionary ecologists study variation and its fitness consequences, but often have difficulties relating behavioural variation to physiological mechanisms. The findings presented here open the possibility that properties of internal, circadian clocks affect performance in traits that are relevant to fitness and sexual selection.
    https://doi.org/10.1098/rspb.2010.0871
  • Ardea
    2010

    Across and within-forest effects on breeding success in Mediterranean Great Tits Parus major

    F. Atiénzar, Marcel E. Visser, J.L. Greño, L.J.M. Holleman, E.J. Belda, E. Barba
    Forest type and habitat structure can have profound effects on different aspects of avian life histories. These effects may, however, strongly differ across and within forests that vary in vegetation composition and structure, especially when an ancient forest has been replaced by a new forest. To test for these differences in effect, we studied Great Tit Parus major life-history traits (280 first clutches) in two Mediterranean evergreen forests during 2005–07: an ancient Holm Oak Quercus ilex and a reforested pine forest. A comparison between forests revealed that females breeding in the Holm Oak forest started laying one week later, and produced larger clutches and broods both at hatching and at fledging. Chicks raised in the Holm Oak forest also fledged in better condition. Within forests, however, the reproductive success was not higher for pairs breeding in nestboxes surrounded by oaks within the pine forest, and also reproductive success was not lower in nestboxes surrounded by pines within oak forest. Instead, vegetation maturity around nestboxes, rather than tree species composition, affected hatching success. Surprisingly, hatching success was higher in nestboxes surrounded by immature vegetation. We suggest that this may be due to a lower nest predation rate in nestboxes surrounded by immature vegetation, compared to nestboxes surrounded by mature vegetation. We suggest that different factors appear to affect variation in breeding success in Mediterranean Great Tits comparing across forests (e.g. food availability) vs. within a forest (e.g. nest predation).
    https://doi.org/10.5253/078.098.0110
  • Evolution
    2010

    Contrasting patterns of phenotypic plasticity in reproductive traits in two great tit (Parus Major) populations

    A. Husby, D.H. Nussey, Marcel E. Visser, A.J. Wilson, Ben C. Sheldon, L.E.B. Kruuk
    Phenotypic plasticity is an important mechanism via which populations can respond to changing environmental conditions, but we know very little about how natural populations vary with respect to plasticity. Here we use random-regression animal models to understand the multivariate phenotypic and genetic patterns of plasticity variation in two key life-history traits, laying date and clutch size, using data from long-term studies of great tits in The Netherlands (Hoge Veluwe [HV]) and UK (Wytham Woods [WW]). We show that, while population-level responses of laying date and clutch size to temperature were similar in the two populations, between-individual variation in plasticity differed markedly. Both populations showed significant variation in phenotypic plasticity (IxE) for laying date, but IxE was significantly higher in HV than in WW. There were no significant genotype-by-environment interactions (GxE) for laying date, yet differences in GxE were marginally nonsignificant between HV and WW. For clutch size, we only found significant IxE and GxE in WW but no significant difference between populations. From a multivariate perspective, plasticity in laying date was not correlated with plasticity in clutch size in either population. Our results suggest that generalizations about the form and cause of any response to changing environmental conditions across populations may be difficult.
    https://doi.org/10.1111/j.1558-5646.2010.00991.x
  • Molecular Ecology
    2010

    Genome-wide SNP detection in the great tit Parus major using high throughput sequencing

    N.E.M. Van Bers, Kees van Oers, H.H.D. Kerstens, B.W. Dibbits, R.P.M.A. Crooijmans, Marcel E. Visser, M.A.M. Groenen
    Identifying genes that underlie ecological traits will open exiting possibilities to study gene–environment interactions in shaping phenotypes and in measuring natural selection on genes. Evolutionary ecology has been pursuing these objectives for decades, but they come into reach now that next generation sequencing technologies have dramatically lowered the costs to obtain the genomic sequence information that is currently lacking for most ecologically important species. Here we describe how we generated over 2 billion basepairs of novel sequence information for an ecological model species, the great tit Parus major. We used over 16 million short sequence reads for the de novo assembly of a reference sequence consisting of 550 000 contigs, covering 2.5%of the genome of the great tit. This reference sequence was used as the scaffold for mapping of the sequence reads, which allowed for the detection of over 20 000 novel single nucleotide polymorphisms. Contigs harbouring 4272 of the single nucleotide polymorphisms could be mapped to a unique location on the recently sequenced zebra finch genome. Of all the great tit contigs, significantly more were mapped to the microchromosomes than to the intermediate and the macrochromosomes of the zebra finch, indicating a higher overall level of sequence conservation on the microchromosomes than on the other types of chromosomes. The large number of great tit contigs that can be aligned to the zebra finch genome shows that this genome provides a valuable framework for large scale genetics, e.g. QTL mapping or whole genome association studies, in passerines.
    https://doi.org/10.1111/j.1365-294X.2009.04486.x
  • Oecologia
    2010

    Temporal differences in food abundance promote coexistence between two congeneric passerines

    T. Veen, Ben C. Sheldon, F.J. Weissing, Marcel E. Visser, A. Qvarnström, G.-P. Sætre
    Many related species share the same environment and utilize similar resources. This is surprising because based on the principle of competitive exclusion one would predict that the superior competitor would drive the other species to extinction; coexistence is only predicted if interspecific competition is weaker than intraspecific competition. Interspecific competition is frequently reduced by differential resource use, resulting in habitat segregation. In this paper, we use the closely related collared and pied flycatcher to assess the potential of habitat differences to affect interspecific competition through a different mechanism, namely by generating temporal differences in availability of similar food resources between the two species. We found that the tree species composition of the breeding territories of the two species differed, mainly by a higher abundance of coniferous species around nest-boxes occupied by pied flycatchers. The temporal availability of caterpillars was measured using frass traps under four deciduous and two coniferous tree species. Deciduous tree species showed an early and narrow peak in abundance, which contrasted with the steady increase in caterpillar abundance in the coniferous tree species through the season. We subsequently calculated the predicted total caterpillar biomass available in each flycatcher territory. This differed between the species, with biomass decreasing more slowly in pied flycatcher territories. Caterpillar biomass is strongly correlated with the reproductive success of collared flycatchers, but much less so with pied flycatchers. However, caterpillar availability can only partly explain the differences in seasonal decline of reproductive success between the two species; we discuss additional factors that may contribute to this species difference. Overall, our results are consistent with the suggestion that minor habitat differences between these two species may contribute to promoting their coexistence.
    https://doi.org/10.1007/s00442-009-1544-1
  • Ethology
    2010

    Singing activity reveals personality traits in great tits

    Marc Naguib, A.M. Kazek, Sonja Schaper, Kees van Oers, Marcel E. Visser
    In animal communication, sexually selected signals have been shown to often signal individual attributes such as motivation or quality. Birdsong is among the best studied signalling systems, and song traits vary substantially among individuals. The question remains if variation in signalling also reflects more general and consistent individual characteristics. Such consistent individual differences in behaviour that are relatively stable over time and contexts are referred to as personality or behavioural syndromes. Here, we studied the relation between singing and explorative behaviour, a well-studied personality trait, using great tits (Parus major) under standardized aviary conditions. The results show that singing activity measured as the number of songs sung in spring prior to breeding correlated with male but not with female explorative behaviour. In contrast, song repertoire was not related to explorative behaviour but varied over the day. The link between explorative and singing behaviour suggests that sexually selected signals are more than signals of quality but can also reflect other intrinsic behavioural characteristics such as personality traits.
    https://doi.org/10.1111/j.1439-0310.2010.01791.x
  • Journal of Avian Biology
    2010

    Similar patterns of age-specific reproduction in an island and mainland population of great tits Parus major

    Sandra Bouwhuis, Arie Van Noordwijk, Ben C. Sheldon, S. Verhulst, Marcel E. Visser
    The process of ageing was long thought to be too infrequent to affect life-histories in natural populations. Long-term studies have, however, recently demonstrated ageing to be ubiquitous even in the wild, although confounding factors, such as emigration instead of mortality, or inter-population variation in rates of ageing have seldom been addressed. Here, we present analyses of female age-specific reproductive performance in a Dutch island population of great tits Parus major. For this population with limited connectivity to surrounding areas, we show that, between individuals, reproductive lifespan positively co-varies with recruit production, while within individuals performance improves up to 3 years of age, after which it gradually declines. We also show these patterns to be strikingly similar to those recently found in a less isolated British mainland population of great tits, characterised by different environmental conditions and life-history strategies, in particular the frequency of multiple breeding. Our results therefore suggest patterns of agespecific reproductive performance to be robust to both environmental and life-history variation.
    https://doi.org/10.1111/j.1600-048X.2010.05111.x
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    2010

    Phenology, seasonal timing and circannual rhythms: towards a unified framework

    Marcel E. Visser, Samuel P. Caro, Kees van Oers, Sonja Schaper, B. Helm
    Phenology refers to the periodic appearance of life-cycle events and currently receives abundant attention as the effects of global change on phenology are so apparent. Phenology as a discipline observes these events and relates their annual variation to variation in climate. But phenology is also studied in other disciplines, each with their own perspective. Evolutionary ecologists study variation in seasonal timing and its fitness consequences, whereas chronobiologists emphasize the periodic nature of life-cycle stages and their underlying timing programmes (e.g. circannual rhythms). The (neuro-) endocrine processes underlying these life-cycle events are studied by physiologists and need to be linked to genes that are explored by molecular geneticists. In order to fully understand variation in phenology, we need to integrate these different perspectives, in particular by combining evolutionary and mechanistic approaches. We use avian research to characterize different perspectives and to highlight integration that has already been achieved. Building on this work, we outline a route towards uniting the different disciplines in a single framework, which may be used to better understand and, more importantly, to forecast climate change impacts on phenology.
    https://doi.org/10.1098/rstb.2010.0111
  • Functional Ecology
    2010

    Maternal effects in an insect herbivore as a mechanism to adapt to host plant phenology

    M. Van Asch, R. Julkunen-Tiito, Marcel E. Visser
    1.Maternal effects may play an important role in shaping the life history of organisms. Using an insect herbivore, the winter moth (Operophtera brumata) feeding on oak (Quercus robur), we show that maternal effects can affect seasonal timing of egg hatching in an herbivore in an adaptive way. 2. Winter moth egg-hatching needs to coincide with oak bud opening, as only freshly emerged leaves are suitable as food for the caterpillars. However, there is spatial variation in the timing of bud opening among oaks to which the winter moth needs to adapt. 3. We show experimentally that the generation time between the mother’s and her offsprings’ hatching dates was shorter for mothers who hatched late relative to bud opening of the tree they had to feed on (and hence had to feed on older leaves) than for mothers’ who hatched on time. Maternal feeding conditions affected both the larval and the pupal development time of the mother as well as the egg development time of her offspring: at all three stages developmental time was shorter for the mistimed treatment. 4.We thus show that adaptation to spatial variation may be achieved via maternal effects. While this is a mechanism selected to adapt to spatial variation, it may now also play a role in adaptation to climate change induced shifts in host phenology, and allow insect herbivores to adapt to changes in the seasonal timing of their food availability without the need for genetic change.
    https://doi.org/10.1111/j.1365-2435.2010.01734.x
  • Journal of Experimental Biology
    2009

    Temperature-induced elevation of basal metabolic rate does not affect testis growth in great tits

    Samuel P. Caro, Marcel E. Visser
    The timing of reproduction varies from year to year in many bird species. To adjust their timing to the prevailing conditions of that year, birds use cues from their environment. However, the relative importance of these cues, such as the initial predictive (e. g. photoperiod) and the supplemental factors (e. g. temperature), on the seasonal sexual development are difficult to distinguish. In particular, the fine-tuning effect of temperature on gonadal growth is not well known. One way temperature may affect timing is via its strong effect on energy expenditure as gonadal growth is an energy-demanding process. To study the interaction of photoperiod and temperature on gonadal development, we first exposed 35 individually housed male great tits (Parus major) to mid-long days (after 6 weeks of 8h L:16 h D at 15 degrees C, photoperiod was set to 13h L:11 h D at 15 degrees C). Two weeks later, for half of the males the temperature was set to 8 degrees C, and for the other half t! o 22 degrees C. Unilateral laparotomies were performed at weeks 5 (i.e one week before the birds were transferred to mid-long days), 8 and 11 to measure testis size. Two measures of basal metabolic rate (BMR) were performed at the end of the experiment (weeks 11 and 12). Testis size increased significantly during the course of the experiment, but independently of the temperature treatment. BMR was significantly higher in birds exposed to the cold treatment. These results show that temperature-related elevation of BMR did not impair the long-day-induced testis growth in great tits. As a consequence, temperature may not be a crucial cue and/or constraint factor in the fine-tuning of the gonadal recrudescence in male great tits, and testis growth is not a high energy-demanding seasonal process.
    https://doi.org/10.1242/jeb.026344
  • Journal of Animal Ecology
    2009

    Spatial and temporal variation in the relative contribution of density dependence, climate variation and migration to fluctuations in the size of great tit populations

    V. Grøtan, B-E. Sæther, S. Engen, J.H. Van Balen, A.C. Perdeck, Marcel E. Visser
    1. The aim of the present study is to model the stochastic variation in the size of five populations of great tit Parus major in the Netherlands, using a combination of individual-based demographic data and time series of population fluctuations. We will examine relative contribution of density-dependent effects, and variation in climate and winter food on local dynamics as well as on number of immigrants. 2. Annual changes in population size were strongly affected by temporal variation in number of recruits produced locally as well as by the number of immigrants. The number of individuals recruited from one breeding season to the next was mainly determined by the population size in year t, the beech crop index (BCI) in year t and the temperature during March–April in year t. The number of immigrating females in year t + 1 was also explained by the number of females present in the population in ye 3. By comparing predictions of the population model with the recorded number of females, the simultaneous modelling of local recruitment and immigration explained a large proportion of the annual variation in recorded population growth rates. 4. Environmental stochasticity especially caused by spring temperature and BCI did in general contribute more to annual fluctuations in population size than density-dependent effects. Similar effects of climate on local recruitment and immigration also caused covariation in temporal fluctuations of immigration and local production of recruits. 5. The effects of various variables in explaining fluctuations in population size were not independent, and the combined effect of the variables were generally non-additive. Thus, the effects of variables causing fluctuations in population size should not be considered separately because the total effect will be influenced by covariances among the explanatory variables. 6. Our results show that fluctuations in the environment affect local recruitment as well as annual fluctuations in the number of immigrants. This effect of environment on the interchange of individuals among populations is important for predicting effects of global climate change on the pattern of population fluctuations.
    https://doi.org/10.1111/j.1365-2656.2008.01488.x
  • Biology Letters
    2009

    Solar activity affects avian timing of reproduction

    Marcel E. Visser, J.J. Sanz
    Avian timing of reproduction is strongly affected by ambient temperature. Here we show that there is an additional effect of sunspots on laying date, from five long-term population studies of great and blue tits (Parus major and Cyanistes caeruleus), demonstrating for the first time that solar activity not only has an effect on population numbers but that it also affects the timing of animal behaviour. This effect is statistically independent of ambient temperature. In years with few sunspots, birds initiate laying late while they are often early in years with many sunspots. The sunspot effect may be owing to a crucial difference between the method of temperature measurements by meteorological stations (in the shade) and the temperatures experienced by the birds. A better understanding of the impact of all the thermal components of weather on the phenology of ecosystems is essential when predicting their responses to climate change.
    https://doi.org/10.1098/rsbl.2009.0429
  • Global Change Biology
    2009

    Climate change leads to decreasing bird migration distances

    Marcel E. Visser, A.C. Perdeck, J.H. Van Balen, Christiaan Both
    Global climate change has led to warmer winters in NW Europe, shortening the distance between suitable overwintering areas and the breeding areas of many bird species. Here we show that winter recovery distances have decreased over the past seven decades, for birds ringed during the breeding season in the Netherlands between 1932 and 2004. Of the 24 species included in the analysis, we found in 12 a significant decrease of the distance to the wintering site. Species from dry, open areas shortened their distance the most, species from wet, open areas the least, while woodland species fall in between the other two habitats. The decline in migration distance is likely due to climate change, as migration distances are negatively correlated with the Dutch temperatures in the winter of recovery. With a shorter migration distance, species should be better able to predict the onset of spring at their breeding sites and this could explain the stronger advancement of arrival date found in several short distance species relative to long-distance migrants.
    https://doi.org/10.1111/j.1365-2486.2009.01865.x
  • Journal of Animal Ecology
    2009

    Climate change and unequal phenological changes across four trophic levels: constraints or adaptations?

    Christiaan Both, M. Van Asch, R.G. Bijlsma, A.B. Van den Burg, Marcel E. Visser
    1. Climate change has been shown to affect the phenology of many organisms, but interestingly these shifts are often unequal across trophic levels, causing a mismatch between the phenology of organisms and their food. 2. We consider two alternative hypotheses: consumers are constrained to adjust sufficiently to the lower trophic level, or prey species react more strongly than their predators to reduce predation. We discuss both hypotheses with our analyses of changes in phenology across four trophic levels: tree budburst, peak biomass of herbivorous caterpillars, breeding phenology of four insectivorous bird species and an avian predator. 3. In our long-term study, we show that between 1988 and 2005, budburst advanced (not significantly) with 0·17 d yr−1, while between 1985 and 2005 both caterpillars (0·75 d year−1) and the hatching date of the passerine species (range for four species: 0·36–0·50 d year−1) have advanced, whereas raptor hatching dates showed no trend. 4. The caterpillar peak date was closely correlated with budburst date, as were the passerine hatching dates with the peak caterpillar biomass date. In all these cases, however, the slopes were significantly less than unity, showing that the response of the consumers is weaker than that of their food. This was also true for the avian predator, for which hatching dates were not correlated with the peak availability of fledgling passerines. As a result, the match between food demand and availabili 5. These results could equally well be explained by consumers' insufficient responses as a consequence of constraints in adapting to climate change, or by them trying to escape predation from a higher trophic level, or both. Selection on phenology could thus be both from matches of phenology with higher and lower levels, and quantifying these can shed new light on why some organisms do adjust their phenology to climate change, while others do not.
    https://doi.org/10.1111/j.1365-2656.2008.01458.x
  • Proceedings of the Royal Society B-Biological Sciences
    2009

    Decline in the frequency and benefits of multiple brooding in great tits as a consequence of a changing environment

    A. Husby, L.E.B. Kruuk, Marcel E. Visser
    For multiple-brooded species, the number of reproductive events per year is a major determinant of an individual's fitness. Where multiple brooding is facultative, its occurrence is likely to change with environmental conditions, and, as a consequence, the current rates of environmental change could have substantial impacts on breeding patterns. Here we examine temporal population-level trends in the proportion of female great tits (Parus major) producing two clutches per year (‘double brooding’) in four long-term study populations in The Netherlands, and show that the proportion of females that double brood has declined in all populations, with the strongest decline taking place in the last 30 years of the study. For one of the populations, for which we have data on caterpillar abundance, we show that the probability that a female produces a second clutch was related to the timing of her first clutch relative to the peak in caterpillar abundance, and that the probability of double brooding declined over the study period. We further show that the number of recruits from the second clutch decreased significantly over the period 1973–2004 in all populations. Our results indicate that adjustment to changing climatic conditions may involve shifts in life-history traits other than simply the timing of breeding.
    https://doi.org/10.1098/rspb.2008.1937
  • Endangered Species Research
    2009

    Travelling through a warming world: climate change and migratory species

    A. Robinson, H.Q.P. Crick, J.A. Learmonth, I.M.D. Maclean, C.D. Thomas, F. Bairlein, M.C. Forchhammer, C.M. Francis, J.A. Gill, B.J. Godley, J. Harwood, G.C. Hays, B. Huntley, A.M. Hutson, G.J. Pierce, M.M. Rehfisch, D.W. Sims, M.C. Vieira dos Santos, T.H. Sparks, D. Stroud, Marcel E. Visser
    Long-distance migrations are among the wonders of the natural world, but this multi-taxon review shows that the characteristics of species that undertake such movements appear to make them particularly vulnerable to detrimental impacts of climate change. Migrants are key components of biological systems in high latitude regions, where the speed and magnitude of climate change impacts are greatest. They also rely on highly productive seasonal habitats, including wetlands and ocean upwellings that, with climate change, may become less food-rich and predictable in space and time. While migrants are adapted to adjust their behaviour with annual changes in the weather, the decoupling of climatic variables between geographically separate breeding and non-breeding grounds is beginning to result in mistimed migration. Furthermore, human land-use and activity patterns will constrain the ability of many species to modify their migratory routes and may increase the stress induced by climate change. Adapting conservation strategies for migrants in the light of climate change will require substantial shifts in site designation policies, flexibility of management strategies and the integration of forward planning for both people and wildlife. While adaptation to changes may be feasible for some terrestrial systems, wildlife in the marine ecosystem may be more dependent on the degree of climate change mitigation that is achievable.
    https://doi.org/10.3354/esr00095
  • Environment International
    2009

    Brominated flame retardants and organochlorines in the European environment using great tit eggs as a biomonitoring tool

    E. Van den Steen, R. Pinxten, V.L.B. Jaspers, A. Covaci, E. Barba, C. Carere, M. Cichoń, A. Dubiec, T. Eeva, P. Heeb, B. Kempenaers, J.T. Lifjeld, T. Lubjuhn, R. Mänd, B. Massa, J-A. Nilsson, A.C. Norte, M. Orell, P. Podzemny, J.J. Sanz, J.C. Senar, J.J. Soler, A. Sorace, J. Török, Marcel E. Visser, W. Winkel, M. Eens
    Large-scale studies are essential to assess the emission patterns and spatial distribution of organohalogenated pollutants (OHPs) in the environment. Bird eggs have several advantages compared to other environmental media which have previously been used to map the distribution of OHPs. In this study, large-scale geographical variation in the occurrence of OHPs, such as polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs) and organochlorine pesticides (OCPs), was investigated throughout Europe using eggs of a terrestrial residential passerine species, the great tit (Parus major). Great tit eggs from 22 sampling sites, involving urban, rural and remote areas, in 14 European countries were collected and analysed (5–8 eggs per sampling site). The environmentally most important congeners/compounds of the analysed pollutants were detectable in all sampling locations. For PCBs, PBDEs and OCPs, no clear geographical contamination pattern was found. Sum PCB levels ranged from 143 ng/g lipid weight (lw) to 3660 ng/g lw. As expected, PCB concentrations were significantly higher in the sampled urban compared to the remote locations. However, the urban locations did not show significantly higher concentrations compared to the rural locations. Sum PBDEs ranged from 4.0 ng/g lw to 136 ng/g lw. PBDEs were significantly higher in the urbanized sampling locations compared to the other locations. The significant, positive correlation between PCB and PBDE concentrations suggests similar spatial exposure and/or mechanisms of accumulation. Significantly higher levels of OCPs (sum OCPs ranging from 191 ng/g lw to 7830 ng/g lw) were detected in rural sampling locations. Contamination profiles of PCBs, PBDEs and OCPs differed also among the sampling locations, which may be due to local usage and contamination sources. The higher variance among sampling locations for the PCBs and OCPs, suggests that local contamination sources are more important for the PCBs and OCPs compared to the PBDEs. To our knowledge, this is the first study in which bird eggs were used as a monitoring tool for OHPs on such a large geographical scale.
    https://doi.org/10.1016/j.envint.2008.08.002
  • Proceedings of the Royal Society B-Biological Sciences
    2009

    Temperature has a causal effect on avian timing of reproduction

    Marcel E. Visser, L.J.M. Holleman, Samuel P. Caro
    Many bird species reproduce earlier in years with high spring temperatures, but little is known about the causal effect of temperature. Temperature may have a direct effect on timing of reproduction but the correlation may also be indirect, for instance via food phenology. As climate change has led to substantial shifts in timing, it is essential to understand this causal relationship to predict future impacts of climate change. We tested the direct effect of temperature on laying dates in great tits (Parus major) using climatized aviaries in a 6-year experiment. We mimicked the temperature patterns from two specific years in which our wild population laid either early (‘warm’ treatment) or late (‘cold’ treatment). Laying dates were affected by temperature directly. As the relevant temperature period started three weeks prior to the mean laying date, with a range of just 4°C between the warm and the cold treatments, and as the birds were fed ad libitum, it is likely that temperature acted as a cue rather than lifting an energetic constraint on the onset of egg production. We furthermore show a high correlation between the laying dates of individuals reproducing both in aviaries and in the wild, validating investigations of reproduction of wild birds in captivity. Our results demonstrate that temperature has a direct effect on timing of breeding, an important step towards assessing the implication of climate change on seasonal timing.
    https://doi.org/10.1098/rspb.2009.0213
  • Oikos
    2008

    Forms of density regulation and (quasi-) stationary distributions of population sizes in birds

    B-E. Sæther, S. Engen, V. Grøtan, T. Bregnballe, Christiaan Both, P. Tryjanowski, A. Leivits, J. Wright, A.P. Møller, Marcel E. Visser, W. Winkel
    The theta-logistic model of density regulation is an especially flexible class of density regulation models where different forms of non-linear density regulation can be expressed by only one parameter, θ. Estimating the parameters of the theta-logistic model is, however, challenging. This is mainly due to the need for information concerning population growth at low densities as well as data on fluctuations around the carrying capacity K in order to estimate the strength of density regulation. Here we estimate parameters of the theta-logistic model for 28 populations of three species of birds that have grown from very small population sizes followed by a period of fluctuations around K. We then use these parameters to estimate the quasi-stationary distribution of population size. There were often large uncertainties in these parameters specifying the form of density regulation that were generally independent of the duration of the study period. In contrast, precision in the estimates of environmental variance increased with the length of the time series. In most of the populations, a large proportion of the probability density of the (quasi-) stationary distribution of population sizes was located at intermediate population sizes relative to K. Thus, we suggest that the (quasi-) stationary distribution of population sizes represents a useful summary statistic that in many cases provides a more robust characterisation of basic population dynamics (e.g. range of variation in population fluctuations or proportion of time spent close to K) than can be obtained from analyses of single model parameters.
    https://doi.org/10.1111/j.0030-1299.2008.16420.x
  • Philosophical Transactions of the Royal Society B: Biological Sciences
    2008

    Introduction. Integration of ecology and endocrinology in avian reproduction: a new synthesis

    J.C. Wingfield, Marcel E. Visser, T.D. Williams
    Birds are some of the most familiar organisms of global ecosystems. Changes in the visibility and abundance of birds are therefore excellent indicators of population and physiological responses to habitat changes and are a major focus for public concern about detrimental environmental changes. In order to understand how birds respond to these challenges, it is essential to determine how the environment affects reproduction under natural conditions. The continuum from environmental variables (cues) to reproductive life-history traits depends upon a cascade of neural and physiological processes that determine the extent and rate at which birds will be able to adapt to changes in their environment. For a full understanding of this ability to adapt, ecologists and endocrinologists need to collaborate and build a common framework. The objective of this theme issue is to bring together a series of papers addressing how evolutionary ecologists and endocrinologists can collaborate directly using avian reproduction as a model system. First, we address the need to integrate ecology and endocrinology and what benefits to biological knowledge will be gained. The papers collected in this issue represent a new synthesis of ecology and endocrinology as discussed in three E-BIRD workshops. The three main foci are trade-offs and constraints, maternal effects and individual variation. Authors within each group present ecological and endocrinological aspects of their topics and many go on to outline testable hypotheses. Finally, we discuss where the major problems remain and how this issue points out where these need collaborative efforts of ecologists and endocrinologists. Specific challenges are raised to future researchers to break through intellectual barriers and explore new frontiers. This framework of topics will ultimately apply to all taxa because the principles involved are universal and hopefully will have direct application to programmes integrating organisms and genes throughout biological sciences.
    https://doi.org/10.1098/rstb.2007.0012
  • Proceedings of the Royal Society B-Biological Sciences
    2008

    Keeping up with a warming world; assessing the rate of adaptation to climate change

    The pivotal question in the debate on the ecological effects of climate change is whether species will be able to adapt fast enough to keep up with their changing environment. If we establish the maximal rate of adaptation, this will set an upper limit to the rate at which temperatures can increase without loss of biodiversity. The rate of adaptation will primarily be set by the rate of microevolution since (i) phenotypic plasticity alone is not sufficient as reaction norms will no longer be adaptive and hence microevolution on the reaction norm is needed, (ii) learning will be favourable to the individual but cannot be passed on to the next generations, (iii) maternal effects may play a role but, as with other forms of phenotypic plasticity, the response of offspring to the maternal cues will no longer be adaptive in Long-term studies on wild populations with individually known animals play an essential role in detecting and understanding the temporal trends in life-history traits, and to estimate the heritability of, and selection pressures on, life-history traits. However, additional measurements on other trophic levels and on the mechanisms underlying phenotypic plasticity are needed to predict the rate of microevolution, especially under changing conditions. Using this knowledge on heritability of, and selection on, life-history traits, in combination with climate scenarios, we will be able to predict the rate of adaptation for different climate scenarios. The final step is to use ecoevolutionary dynamical models to make the link to population viability and from there to biodiversity loss for those scenarios where the rate of adaptation is insufficient.
    https://doi.org/10.1098/rspb.2007.0997
  • PLoS One
    2007

    Great Tits (Parus major) reduce caterpillar damage in commercial apple orchards

    C.M.M. Mols, Marcel E. Visser
    Alternative ways to control caterpillar pests and reduce the use of pesticides in apple orchards are in the interest of the environment, farmers and the public. Great tits have already been shown to reduce damage under high caterpillar density when breeding in nest boxes in an experimental apple orchard. We tested whether this reduction also occurs under practical conditions of Integrated Pest Management (IPM), as well as Organic Farming (OF), by setting up an area with nest boxes while leaving a comparable area as a control within 12 commercial orchards. We showed that in IPM orchards, but not in OF orchards, in the areas with breeding great tits, apples had 50% of the caterpillar damage of the control areas. Offering nest boxes to attract insectivorous passerines in orchards can thus lead to more limited pesticide use, thereby adding to the natural biological diversity in an agricultural landscape, while also being economically profitable to the fruit growers.
    https://doi.org/10.1371/journal.pone.0000202
  • Journal of Animal Ecology
    2007

    The extended Moran effect and large-scale synchronous fluctuations in the size of great tit and blue tit populations

    B-E. Sæther, S. Engen, V. Grøtan, W. Fiedler, E. Matthysen, Marcel E. Visser, J. Wright, A.P. Møller, F. Adriaensen, H. van Balen, D. Balmer, M.C. Mainwaring, R. McCleery, M. Pampus, W. Winkel
    1. Synchronous fluctuations of geographically separated populations are in general explained by the Moran effect, i.e. a common influence on the local population dynamics of environmental variables that are correlated in space. Empirical support for such a Moran effect has been difficult to provide, mainly due to problems separating out effects of local population dynamics, demographic stochasticity and dispersal that also influence the spatial scaling of population processes. Here we generalize the Moran effect by decomposing the spatial autocorrelation function for fluctuations in the size of great tit Parus major and blue tit Cyanistes caeruleus populations into components due to spatial correlations in the environmental noise, local differences in the strength of density regulation and the effects of demographic stochasticity. 2. Differences between localities in the strength of density dependence and nonlinearity in the density regulation had a small effect on population synchrony, whereas demographic stochasticity reduced the effects of the spatial correlation in environmental noise on the spatial correlations in population size by 21·7% and 23·3% in the great tit and blue tit, respectively. 3. Different environmental variables, such as beech mast and climate, induce a common environmental forcing on the dynamics of central European great and blue tit populations. This generates synchronous fluctuations in the size of populations located several hundred kilometres apart. 4. Although these environmental variables were autocorrelated over large areas, their contribution to the spatial synchrony in the population fluctuations differed, dependent on the spatial scaling of their effects on the local population dynamics. We also demonstrate that this effect can lead to the paradoxical result that a common environmental variable can induce spatial desynchronization of the population fluctuations. 5. This demonstrates that a proper understanding of the ecological consequences of environmental changes, especially those that occur simultaneously over large areas, will require information about the spatial scaling of their effects on local population dynamics.
    https://doi.org/10.1111/j.1365-2656.2006.01195.x
  • Global Change Biology
    2007

    Predicting adaptation of phenology in response to climate change, an insect herbivore example

    M. Van Asch, P.H. Van Tienderen, L.J.M. Holleman, Marcel E. Visser
    Climate change has led to an advance in phenology in many species. Synchrony in phenology between different species within a food chain may be disrupted if an increase in temperature affects the phenology of the different species differently, as is the case in the winter moth egg hatch–oak bud burst system. Operophtera brumata (winter moth) egg hatch date has advanced more than Quercus robur (pedunculate oak) bud burst date over the past two decades. Disrupted synchrony will lead to selection, and a response in phenology to this selection may lead to species genetically adapting to their changing environment. However, a prerequisite for such genetic change is that there is sufficient genetic variation and severe enough fitness consequences. So far, examples of observed genetic change have been few. Using a half-sib design, we demonstrate here that O. brumata egg-hatching reaction norm is heritable, and that genetic variation exists. Fitness consequences of even a few days difference between egg hatch and tree bud opening are severe, as we experimentally determined. Estimates of genetic variation and of fitness were then combined with a climate scenario to predict the rate and the amount of change in the eggs' response to temperature. We predict a rapid response to selection, leading to a restoration of synchrony of egg hatch with Q. robur bud opening. This study shows that in this case there is a clear potential to adapt – rapidly – to environmental change. The current observed asynchrony is therefore not due to a lack of genetic variation and at present it is unclear what is constraining O. brumata to adapt. This kind of model may be particularly useful in gaining insight in the predicted amount and rate of change due to environmental changes, given a certain genetic variation and selection pressure.
    https://doi.org/10.1111/j.1365-2486.2007.01400.x
  • Annual Review of Entomology
    2007

    Phenology of forest caterpillars and their host trees: The importance of synchrony

    M. Van Asch, Marcel E. Visser
    For many leaf-feeding herbivores, synchrony in phenology with their host plant is crucial as development outside a narrow phenological time window has severe fitness consequences. In this review, we link mechanisms, adaptation, and population dynamics within a single conceptual framework, needed for a full understanding of the causes and consequences of this synchrony. The physiological mechanisms underlying herbivore and plant phenology are affected by environmental cues, such as photoperiod and temperature, although not necessarily in the same way. That these different mechanisms lead to synchrony, even if there is spatial and temporal variation in plant phenology, is a result of the strong natural selection acting on the mechanism underlying herbivore phenology. Synchrony has a major impact on the population densities of leaf-feeding Lepidoptera, and years with a high synchrony may lead to outbreaks. Global climate change leads to a disruption of the synchrony between herbivores and their host plants, which may have major impacts for population viability if natural selection is insufficient to restore synchrony.
    https://doi.org/10.1146/annurev.ento.52.110405.091418
  • Functional Ecology
    2006

    Possible fitness consequences of experimentally advanced laying dates in Great Tits: differences between populations in different habitats

    Phillip Gienapp, Marcel E. Visser
    1. In birds, early breeding individuals generally reproduce more successfully than late breeding individuals. The lack of response to this selection could be explained by resource constraints during the egg production period. 2. Parus species can learn from the mismatch experienced between breeding time and nestling food availability and subsequently adjust their breeding time accordingly. In two Great Tit populations, breeding time was manipulated by creating an artificial food peak. This allowed us to study fitness consequences of manipulated breeding time in the following year without the confounding effects of food supplementation. 3. In one population, manipulated females advanced their laying dates in response to the artificial food peak. However, sample sizes were too low to quantify fitness consequences. In the other population, no response to the treatment was found. This difference could be caused by differences in resource availability in early spring between the two habitats. Low resource availability in early spring could also explain the lack of response to selection observed in one population [KEYWORDS: Climate change ; food supplementation ; Parus major ; resource constraints ; selection on breeding time]
    https://doi.org/10.1111/j.1365-2435.2006.01079.x
  • Oecologia
    2006

    Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird

    Marcel E. Visser, L.J.M. Holleman, Phillip Gienapp
    Timing of reproduction has major fitness consequences, which can only be understood when the phenology of the food for the offspring is quantified. For insectivorous birds, like great tits (Parus major), synchronisation of their offspring needs and abundance of caterpillars is the main selection pressure. We measured caterpillar biomass over a 20-year period and showed that the annual peak date is correlated with temperatures from 8 March to 17 May. Laying dates also correlate with temperatures, but over an earlier period (16 March – 20 April). However, as we would predict from a reliable cue used by birds to time their reproduction, also the food peak correlates with these temperatures. Moreover, the slopes of the phenology of the birds and caterpillar biomass, when regressed against the temperatures in this earlier period, do not differ. The major difference is that due to climate change, the relationship between the timing of the food peak and the temperatures over the 16 March – 20 April period is changing, while this is not so for great tit laying dates. As a consequence, the synchrony between offspring needs and the caterpillar biomass has been disrupted in the recent warm decades. This may have severe consequences as we show that both the number of fledglings as well as their fledging weight is affected by this synchrony. We use the descriptive models for both the caterpillar biomass peak as for the great tit laying dates to predict shifts in caterpillar and bird phenology 2005–2100, using an IPCC climate scenario. The birds will start breeding earlier and this advancement is predicted to be at the same rate as the advancement of the food peak, and hence they will not reduce the amount of the current mistiming of about 10 days. [KEYWORDS: Climate change ; Fitness ; Great tit ; Phenology ; Timing of reproduction]
    https://doi.org/10.1007/s00442-005-0299-6
  • Evolution
    2006

    Why breeding time has not responded to selection for earlier breeding in a songbird population

    Phillip Gienapp, E. Postma, Marcel E. Visser
    A crucial assumption underlying the breeders' equation is that selection acts directly on the trait of interest, and not on an unmeasured environmental factor which affects both fitness and the trait. Such an environmentally induced covariance between a trait and fitness has been repeatedly proposed as an explanation for the lack of response to selection on avian breeding time. We tested this hypothesis using a long-term dataset from a Dutch great tit (Parus major) population. Although there was strong selection for earlier breeding in this population, egg-laying dates have changed only marginally over the last decades. Using a so-called animal model, we quantified the additive genetic variance in breeding time and predicted breeding values for females. Subsequently, we compared selection at the phenotypic and genetic levels for two fitness components, fecundity and adult survival. We found no evidence for an environmentally caused covariance between breeding time and fitness or counteracting selection on the different fitness components. Consequently, breeding time should respond to selection but the expected response to selection was too small to be detected.
    https://doi.org/10.1554/06-235.1
  • Acta Zoologica Sinica
    2006

    Mistimed reproduction due to global climate change

    Marcel E. Visser, Christiaan Both, Phillip Gienapp
  • Ardea
    2006

    Pied Flycatchers Ficedula hypoleuca travelling from Africa to breed in Europe: differential effects of winter and migration conditions on breeding date

    Christiaan Both, J.J. Sanz, A.V. Artemyev, B. Blaauw, R.J. Cowie, A.J. Dekhuijzen, A. Enemar, A. Järvinen, N.E.I. Nyholm, J. Potti, P.-A. Ravussin, B. Silverin, F.M. Slater, L.V. Sokolov, Marcel E. Visser, W. Winkel, J. Wright, H. Zang
    In most bird species there is only a short time window available for optimal breeding due to variation in ecological conditions in a seasonal environment. Long-distance migrants must travel before they start breeding, and conditions at the wintering grounds and during migration may affect travelling speed and hence arrival and breeding dates. These effects are to a large extent determined by climate variables such as rainfall and temperature, and need to be identified to predict how well species can adapt to climate change. In this paper we analyse effects of vegetation growth on the wintering grounds and sites en route on the annual timing of breeding of 17 populations of Pied Flycatchers Ficedula hypoleuca studied between 1982–2000. Timing of breeding was largely correlated with local spring temperatures, supplemented by striking effects of African vegetation and NAO. Populations differed in the effects of vegetation growth on the wintering grounds, and on their northern African staging grounds, as well as ecological conditions in Europe as measured by the winter NAO. In general, early breeding populations (low altitude, western European populations) bred earlier in years with more vegetation in the Northern Sahel zone, as well as in Northern Africa. In contrast, late breeding populations (high altitude and northern and eastern populations) advanced their breeding dates when circumstances in Europe were more advanced (high NAO). Thus, timing of breeding in most Pied Flycatcher populations not only depends upon local circumstances, but also on conditions encountered during travelling, and these effects differ across populations dependent on the timing of travelling and breeding.
  • Acta Biotheoretica
    2006

    Analysing population numbers of the House Sparrow in the Netherlands with a matrix model and suggestions for conservation measures

    C. Klok, R. Holtkamp, R. van Apeldoorn, Marcel E. Visser, L. Hemerik
    The House Sparrow (Passer domesticus), formerly a common bird species, has shown a rapid decline in Western Europe over recent decades. In The Netherlands, its decline is apparent from 1990 onwards. Many causes for this decline have been suggested that all decrease the vital rates, i.e. survival and reproduction, but their actual impact remains unknown. Although the House Sparrow has been dominant in The Netherlands, data on life history characteristics for this bird species are scarce: data on reproduction are non-existent, and here we first present survival estimates based on live encounters and dead recoveries of marked individuals over the period 1976–2003, 14 years before and 14 years during the decline, reported to the Dutch Ringing Centre. We show that there is an indication that both juvenile and adult survival are lower during the period of decline. Secondly, to be able to analyse the relative impact of changes in the vital rates, we formulated a general matrix model based on a range of survival values between zero and one with a step size of 0.01 (both juvenile and adult yearly survival) and a range of realistic reproduction values (one, three or five fledglings per pair per year). With the matrix model, we calculated the finite rate of population change (λ) and applied elasticity analysis. To diagnose the cause of the decline in the Dutch
    https://doi.org/10.1007/s10441-006-7871-2
  • Acta Zoologica Sinica
    2006

    Integrating the avian annual cycle

    B. Helm, Marcel E. Visser
  • Ecology
    2005

    Time to extinction of bird populations

    B-E. Sæther, S. Engen, A.P. Møller, Marcel E. Visser, E. Matthysen, W. Fiedler, M.M. Lambrechts, P.H. Becker, J.E. Brommer, J. Dickinson, C. du Feu, F.R. Gehlbach, J. Merilä, W. Rendell, R.J. Robertson, D.L. Thomson, J. Török
    The risk of extinction of populations has not previously been empirically related to parameters characterizing their population dynamics. To analyze this relationship, we simulated how the distribution of population dynamical characters changed as a function of time, in both the remaining and the extinct populations. We found for a set of 38 bird populations that environmental stochasticity had the most immediate effect on the risk of extinction, whereas the long-term persistence of the population was most strongly affected by the specific population growth rate. This illustrates the importance of including information on temporal trends in population size when assessing the viability of a population. We used these relationships to examine whether time to extinction can be predicted from interspecific life history variation. Two alternative hypotheses were examined. (1) Time to extinction should decrease with increasing clutch size or decreasing survival rate because of the larger stochastic components in the population dynamics of such species. (2) Time to extinction should increase with decreasing clutch size or longer life expectancy if extinction rates are most strongly influenced by variation in the specific population growth rate. In the present data set, time to extinction increased with decreasing clutch size because of larger stochastic influences on the population dynamics of species with large clutch sizes located toward the fast end of the “slow–fast continuum” of life history variation. This demonstrates that interspecific variation in extinction risk can be predicted from knowledge of general life history characteristics. Such information can therefore be useful for assessing minimum sizes of viable populations of birds. [KEYWORDS: birds; clutch size; comparative analyses; demography; environmental stochasticity; life history variation; PVA; stochastic population dynamics; population growth rate; time to extinction; viable population size]
    https://doi.org/10.1890/04-0878
  • Ardea
    2005

    Assessing the reduction of caterpillar numbers by Great Tits Parus major breeding in apple orchards

    C.M.M. Mols, Arie Van Noordwijk, Marcel E. Visser
    Great Tits Parus major can reduce fruit damage in apple orchards by predating on caterpillars. A model by Mols (2003) predicted that damage reduction is mainly influenced by the hatching date of the Great Tit nestlings and the number of breeding pairs in the orchard. We tested these predictions by investigating predation pressure on caterpillars by Great Tits in various orchards. First we calculated the total number of feeding visits by Great Tits using two different methods: event counters and the daily weight gain of nestlings. For the latter method we needed to make assumptions on prey size selectivity of Great Tits to prevent overestimation of the number of visits. With the event counters we showed that the number of feeding visits increased with date and with the number of nestlings but there was no effect of hatching date on the total number of feeds over the whole nesting period. Next, we used these data on feeding visits to calculate the maximum proportion of caterpillars that Great Tits removed in organic apple orchards. The average number of three breeding pairs of Great Tits per ha removed on average 23% of the caterpillars. This percentage can increase up to 49% if all foraging takes place within the orchard.
  • Global Change Biology
    2005

    The effect of climate change on the correlation between avian life history traits

    Christiaan Both, Marcel E. Visser
    The ultimate reason why birds should advance their phenology in response to climate change is to match the shifting phenology of underlying levels of the food chain. In a seasonal environment, the timing of food abundance is one of the crucial factors to which birds should adapt their timing of reproduction. They can do this by shifting egg-laying date (LD), and also by changing other life-history characters that affect the period between laying of the eggs and hatching of the chicks. In a long-term study of the migratory Pied Flycatcher, we show that the peak of abundance of nestling food (caterpillars) has advanced during the last two decades, and that the birds advanced their LD. LD strongly correlates with the timing of the caterpillar peak, but in years with an early food peak the birds laid their eggs late relative to this food peak. In such years, the birds advance their hatching date by incubating earlier in the clutch and reducing the interval between laying the last egg to hatching of the first egg, thereby partly compensating for their relative late LD. Paradoxically, they also laid larger clutches in the years with an early food peak, and thereby took more time to lay (i.e. one egg per day). Clutch size therefore declined more strongly with LD in years with an early food peak. This stronger response is adaptive because the fitness of an egg declined more strongly with date in early than in late years. Clearly, avian life-history traits are correlated and Pied Flycatchers apparently optimize over the whole complex of the traits including LD, clutch size and the onset of incubation. Climate change will lead to changing selection pressures on this complex of traits and presumably the way they are correlated. [KEYWORDS: climate change ; clutch size ; Ficedula hypoleuca ; food availability ; laying date]
    https://doi.org/10.1111/j.1365-2486.2005.01038.x
  • Proceedings of the Royal Society B-Biological Sciences
    2005

    Shifts in phenology due to global climate change: the need for a yardstick

    Marcel E. Visser, Christiaan Both
    Climate change has led to shifts in phenology in many species distributed widely across taxonomic groups. It is, however, unclear how we should interpret these shifts without some sort of a yardstick: a measure that will reflect how much a species should be shifting to match the change in its environment caused by climate change. Here, we assume that the shift in the phenology of a species' food abundance is, by a first approximation, an appropriate yardstick. We review the few examples that are available, ranging from birds to marine plankton. In almost all of these examples, the phenology of the focal species shifts either too little (five out of 11) or too much (three out of 11) compared to the yardstick. Thus, many species are becoming mistimed due to climate change. We urge researchers with long-term datasets on phenology to link their data with those that may serve as a yardstick, because documentation of the incidence of climate change-induced mistiming is crucial in assessing the impact of global climate change on the natural world. [KEYWORDS: phenology ; climate change ; mistiming ; food chains]
    https://doi.org/10.1098/rspb.2005.3356
  • Nature
    2005

    Generation time and temporal scaling of bird population dynamics

    B-E. Sæther, R. Lande, S. Engen, H. Weimerskirch, M. Lillegård, R. Altwegg, P.H. Becker, T. Bregnballe, J.E. Brommer, R. McCleery, J. Merilä, E. Nyholm, W. Rendell, R.J. Robertson, P. Tryjanowski, Marcel E. Visser
    https://doi.org/10.1038/nature03666
  • Science Magazine
    2005

    Selection on heritable phenotypic plasticity in a wild bird population

    D.H. Nussey, E. Postma, Phillip Gienapp, Marcel E. Visser
    Theoretical and laboratory research suggests that phenotypic plasticity can evolve under selection. However, evidence for its evolutionary potential from the wild is lacking. We present evidence from a Dutch population of great tits (Parus major) for variation in individual plasticity in the timing of reproduction, and we show that this variation is heritable. Selection favoring highly plastic individuals has intensified over a 32-year period. This temporal trend is concurrent with climate change causing a mismatch between the breeding times of the birds and their caterpillar prey. Continued selection on plasticity can act to alleviate this mismatch.
    https://doi.org/10.1126/science.1117004
  • Global Change Biology
    2005

    A new statistical tool to predict phenology under climate change scenarios

    Phillip Gienapp, L. Hemerik, Marcel E. Visser
    Climate change will likely affect the phenology of trophic levels differently and thereby disrupt the phenological synchrony between predators and prey. To predict this disruption of the synchrony under different climate change scenarios, good descriptive models for the phenology of the different species are necessary. Many phenological models are based on regressing the observed phenological event against temperatures measured over a fixed period. This is problematic, especially when used for future predictions because the paradoxical situation could arise that the phenological event occurs before the period over which temperature is measured. Such models are unable to predict population variation in phenology. Here, we propose a 'proportional hazards model' to describe phenology and illustrate it with an example from breeding time in birds. This type of model circumvents the above-mentioned problems and is generally applicable for describing phenology, which is essential when assessing the ecological impact of climate change. [KEYWORDS: climate change ; descriptive models ; egg laying dates ; Parus major ; phenology ; proportional hazards model]
    https://doi.org/10.1111/j.1365-2486.2005.00925.x
  • Journal of Avian Biology
    2005

    Climatic effects on timing of spring migration and breeding in a long-distance migrant, the pied flycatcher Ficedula hypoleuca

    Christiaan Both, R.G. Bijlsma, Marcel E. Visser
    Climate change has advanced the breeding dates of many bird species, but for few species we know whether this advancement is sufficient to track the advancement of the underlying levels of the food chain. For the long-distance migratory pied flycatcher Ficedula hypoleuca the advancement in breeding time has been insufficient to maintain the synchrony with their main food sources. The timing of arrival in the breeding areas from their African wintering grounds is likely to constrain the advancement of breeding date. We hypothesise that this is because in Africa they cannot predict the advancement of spring in their breeding habitat. However, long-distance migrants may advance their arrival time by migrating faster when circumstances en route are favourable. In this study we show that both arrival and breeding date depend on temperatures at their main North African staging grounds, as well as on temperature at the breeding grounds. Male arrival and average laying date were not correlated, but the positive effect of temperature in North Africa on breeding dates suggests that breeding date is indeed constrained by arrival of females. Long-distance migrants thus are able to adjust arrival and hence breeding by faster spring migration, but the degree of adjustment is probably limited as timing schedules in spring are tight. Furthermore, as climate change is affecting temperatures differently along the migratory flyway and the breeding areas, it is unlikely that arrival dates are advanced at the same rate as the timing of breeding should advance, given the advancement of the underlying levels of the food chain.
    https://doi.org/10.1111/j.0908-8857.2005.03484.x
  • American Naturalist
    2004

    Life-History variation predicts the effects of demographic stochasticity on avian population Dynamics

    B-E. Sæther, S. Engen, A.P. Møller, H. Weimerskirch, Marcel E. Visser, W. Fiedler, E. Matthysen, M.M. Lambrechts, A. Badyaev, P.H. Becker, J.E. Brommer, D. Bukacinski, M. Bukacinski, H. Christensen, J. Dickinson, C. du Feu, F.R. Gehlbach, D. Heg, H. Hötker, J. Merilä, J.T. Nielsen, W. Rendell, R.J. Robertson, D.L. Thomson, J. Török, P. van Hecke
    Comparative analyses of avian population fluctuations have shown large interspecific differences in population variability that have been difficult to relate to variation in general ecological characteristics. Here we show that interspecific variation in demographic stochasticity, caused by random variation among individuals in their fitness contributions, can be predicted from a knowledge of the species' position along a "slow-fast" gradient of life-history variation, ranging from high reproductive species with short life expectancy at one end to species that often produce a single offspring but survive well at the other end of the continuum. The demographic stochasticity decreased with adult survival rate, age at maturity, and generation time or the position of the species toward the slow end of the slow-fast life-history gradient. This relationship between life-history characteristics and demographic stochasticity was related to interspecific differences in the variation among females in recruitment as well as to differences in the individual variation in survival. Because reproductive decisions in birds are often subject to strong natural selection, our results provide strong evidence for adaptive modifications of reproductive investment through life-history evolution of the influence of stochastic variation on avian population dynamics. [KEYWORDS: demographic stochasticity ; environmental stochasticity ; life-history variation ; stochastic population dynamics ; birds]
    https://doi.org/10.1086/425371
  • Proceedings of the Royal Society B-Biological Sciences
    2004

    Large-scale geographical variation confirms that climate change causes birds to lay earlier

    Christiaan Both, A.V. Artemyev, B. Blaauw, R.J. Cowie, A.J. Dekhuijzen, T. Eeva, A. Enemar, L. Gustafsson, E.V. Ivankina, A. Järvinen, N.B. Metcalfe, N.E.I. Nyholm, J. Potti, P.-A. Ravussin, J.J. Sanz, B. Silverin, F.M. Slater, L.V. Sokolov, J. Török, W. Winkel, J. Wright, H. Zang, Marcel E. Visser
    Advances in the phenology of organisms are often attributed to climate change, but alternatively, may reflect a publication bias towards advances and may be caused by environmental factors unrelated to climate change. Both factors are investigated using the breeding dates of 25 long-term studied populations of Ficedula flycatchers across Europe. Trends in spring temperature varied markedly between study sites, and across populations the advancement of laying date was stronger in areas where the spring temperatures increased more, giving support to the theory that climate change causally affects breeding date advancement. [KEYWORDS: life history, laying date, clutch size, climate change, Ficedula hypoleuca, Ficedula albicollis]
    https://doi.org/10.1098/rspb.2004.2770
  • Proceedings of the Royal Society B-Biological Sciences
    2004

    Central assumptions of predator-prey models fail in a semi-natural experimental system

    C.M.M. Mols, Kees van Oers, L.M.A. Witjes, Kate Lessells, P.J. Drent, Marcel E. Visser
    The relationship between the encounter rate of predators with prey and the density of this prey is fundamental to models of predator-prey interactions. The relationship determines, among other variables, the rate at which prey patches are depleted, and hence the impact of predator populations on their prey, and the optimal spatial distribution of foraging effort. Two central assumptions that are made in many models are that encounter rate is directly proportional to prey density and that it is independent of the proportion of prey already removed, other than via the decreased density. We show here, using captive great tits searching for winter moth caterpillars in their natural hiding positions, that neither of these assumptions hold. Encounter rate increased less than directly in proportion to prey density, and it depended not only on the current density of prey, but also on the proportion of prey already removed by previous foragers. Both of these effects are likely to have major consequences for the outcome of predator-prey interactions.
    https://doi.org/10.1098/rsbl.2003.0110
  • Proceedings of the Royal Society B-Biological Sciences
    2003

    Variable responses to large-scale climate change in European Parus populations

    Marcel E. Visser, F. Adriaensen, J.H. Van Balen, J. Blondel, A.A. Dhondt, S. Van Dongen, C. du Feu, E.V. Ivankina, A. Kerimov, J. De Laet, E. Matthysen, R. McCleery, M. Orell, D.L. Thomson
    Spring temperatures in temperate regions have increased over the past 20 years and many organisms have responded to this increase by advancing the timing of their growth and reproduction. However, not all populations show an advancement of phenology. Understanding why some populations advance and others do not will give us insight into the possible constraints and selection pressures on the advancement of phenology. By combining two decades of data on 24 populations of tits (Parus sp.) from six European countries, we show that the phenological response to large-scale changes in spring temperature varies across a species' range, even between populations situated close to each other. We show that this variation cannot be fully explained by variation in the temperature change during the pre- and post-laying periods, as recently suggested. Instead, we find evidence for a link between rising temperatures and the frequency of second broods, which results in complex shifts in the laying dates of first clutches. Our results emphasize the need to consider links between different life-history parameters in order to predict the ecological consequences of large-scale climate changes.
    https://doi.org/10.1098/rspb.2002.2244
  • Proceedings of the Royal Society B-Biological Sciences
    2003

    Climate variation and regional gradients in population dynamics of two hole-nesting passerines

    B-E. Sæther, S. Engen, A.P. Møller, E. Matthysen, F. Adriaensen, W. Fiedler, A. Leivits, M.M. Lambrechts, Marcel E. Visser, T. Anker-Nilssen, Christiaan Both, A.A. Dhondt, R. McCleery, J. McMeeking, J. Potti, O.W. Røstad, D.L. Thomson
    Latitudinal gradients in population dynamics can arise through regional variation in the deterministic components of the population dynamics and the stochastic factors. Here, we demonstrate an increase with latitude in the contribution of a large-scale climate pattern, the North Atlantic Oscillation (NAO), to the fluctuations in size of populations of two European hole-nesting passerine species. However, this influence of climate induced different latitudinal gradients in the population dynamics of the two species. In the great tit the proportion of the variability in the population fluctuations explained by the NAO increased with latitude, showing a larger impact of climate on the population fluctuations of this species at higher latitudes. In contrast, no latitudinal gradient was found in the relative contribution of climate to the variability of the pied flycatcher populations because the total environmental stochasticity increased with latitude. This shows that the population ecological consequences of an expected climate change will depend on how climate affects the environmental stochasticity in the population process. In both species, the effects will be larger in those parts of Europe where large changes in climate are expected.
    https://doi.org/10.1098/rspb.2003.2499
  • American Naturalist
    2003

    Density dependence, territoriality, and divisibility of resources: From optimality models to population processes

    Christiaan Both, Marcel E. Visser
    Species differ enormously in their territorial systems. Some species defend only small areas surrounded by undefended space, while others defend large contiguous territories. Using an optimization approach, we show that this variation can be explained from the density of two types of resources: divisible and nondivisible. We assume that benefits of territories are monotonously related to the defended amount of divisible resources (hereafter called food). In contrast, no benefits are obtained without a nondivisible resource (hereafter called nest site) in the territory, while more than one nest site does not further increase the benefits. The optimal territory size depends on the relative abundance of these resources. With a low density of nest sites, the optimal territory size is small and includes only the nest site. If the density of nest sites is relatively large, the optimal territory size is high, and territories are contiguous. Competition for these different resources yields contrasting patterns of how populations are regulated. If there is mainly competition for nest sites, we expect density-dependent exclusion through territoriality and no density-dependent reproduction. When competition is mainly for food, we expect density-dependent reproduction because optimal territory size will be compressed at higher densities, resulting in lower reproductive success. These predicted patterns indeed are observed in some well-studied passerine species for which both the territorial system and the occurrence of density dependence is known. [KEYWORDS: dependence, territory, divisible resource, optimality model, nest site, bird]
    https://doi.org/10.1086/346098
  • Journal of Applied Ecology
    2002

    Great tits can reduce caterpillar damage in apple orchards

    C.M.M. Mols, Marcel E. Visser
    1.The potential contribution of vertebrate predators to biological control in orchards has been largely overlooked to date. A few studies have shown that birds reduce numbers of pests, but data are scarce on the effects on the pattern or timing of damage. Consequently, the practical value of birds as biocontrol agents remains unclear. 2. This study considered whether great tits Parus major can reduce caterpillar numbers and fruit damage by caterpillars, and increase biological yield, in an experimental orchard of apple trees with high caterpillar numbers. The outcome would depend on the coincidence of the period during which great tits forage and the period during which caterpillars cause damage. In the first experiment nets were put over trees at different times of the growing season, thus creating different periods during 3. The longer the period of foraging by great tits, from the start of egg incubation until fledging of young, the less the overall pest damage to fruit. Damage caused by caterpillars was greater the later they were removed, from the young apple stage onwards. 4. The effect of great tits on caterpillar damage to apples was small (percentage damage was reduced from 13·8% to 11·2%) but significant (P <0·05), and the yield of fruit increased significantly (from 4·7 to 7·8 kg apples per tree, P<0·05). The only cost to the producer was that of erecting nest boxes (c. 2 ha1) to encourage great tits to breed in the orchard. Depending on the great tits' numeric response to insect densities, their relative impact may be greater at lower densities more typi
    https://doi.org/10.1046/j.1365-2664.2002.00761.x
  • Science Magazine
    2002

    Evidence for the effect of learning on timing of reproduction in blue tits

    F. Grieco, Arie Van Noordwijk, Marcel E. Visser
    We experimentally show that in blue tits (Parus caeruleus) egg-laying date is causally linked to experience in the previous year. Females that received additional food in the nestling period in one year laid eggs later in the next year compared with the control birds, whatever the degree of synchronization with the natural food abundance in the previous year. As a result, they raised their brood much later than the peak period of nestling food availability in the next year. The response to experience is adaptive for blue tits, which live in heterogeneous habitats where the peak period of food varies, but once settled will breed at the same location for life. [KEYWORDS: BIRDS]
    https://doi.org/10.1126/science.1068287
  • Oikos
    2002

    Density dependence and stochastic variation in a newly established population of a smal songbird

    B-E. Sæther, S. Engen, R. Lande, Christiaan Both, Marcel E. Visser
    Models describing fluctuations in population size should include both density dependence and stochastic effects. We examine the relative contribution of variation in parameters of the expected dynamics as well as demographic and environmental stochasticity to fluctuations in a population of a small passerine bird, the pied flycatcher, that was newly established in a Dutch study area. Using the theta-logistic model of density regulation, we demonstrate that the estimated quasi-stationary distribution including demographic stochasticity is close to the stationary distribution ignoring demographic stochasticity, indicating a long expected time to extinction. We also show that the variance in the estimated quasi-stationary distribution is especially sensitive to variation in the density regulation function. Reliable population projections must therefore account for uncertainties in parameter estimates which we do by using the population prediction interval (PPI). After 2 years the width of the 90% PPI was already larger than the corresponding estimated range of variation in the quasi-stationary distribution. More precise prediction of future population size than can be derived from the quasi-stationary distribution could only be made for a time span less than about five years.
    https://doi.org/10.1034/j.1600-0706.2002.990214.x
  • Proceedings of the Royal Society B-Biological Sciences
    2001

    Warmer springs disrupt the synchrony of oak and winter moth phenology

    Marcel E. Visser, L.J.M. Holleman
    Spring temperatures have increased over the past 25 years, to which a wide variety of organisms have responded. The outstanding question is whether these responses match the temperature-induced shift of the selection pressures acting on these organisms. Organisms have evolved response mechanisms that are only adaptive given the existing, relationship between the cues organisms use and the selection pressures acting on them. Global warming may disrupt ecosystem interactions because it alters these relationships and micro-evolution may be slow in tracking these changes. In particular, such shifts have serious consequences for ecosystem functioning for the tight multitrophic interactions involved in the timing of reproduction and growth. We determined the response of winter moth (Operophtera brumata) egg hatching and oak (Quercus robur) bud burst to temperature, a system with strong selection on synchronization. We show that there has been poor synchrony in recent warm springs, which is due to an increase in spring temperatures without a decrease in the incidence of freezing spells in winter. This is a clear warning that such changes in temperature patterns may affect ecosystem interactions more strongly than changes in mean temperature. [KEYWORDS: timing; phenotypic plasticity; Operophtera brumata; Quercus robur; climate change; multitrophic interaction Operophtera-brumata l; egg-laying trends; climate change; quercus-robur; elevated-temperature; larval emergence; pedunculate oak; budburst; trees; caterpillars]
    https://doi.org/10.1098/rspb.2000.1363
  • Nature
    2001

    Adjustment to climate change is constrained by arrival date in a long-distance migrant bird

    Christiaan Both, Marcel E. Visser
    Spring temperatures in temperate regions have increased over the past 20 years(1), and many organisms have responded to this increase by advancing the date of their growth and reproduction(2-7). Here we show that adaptation to climate change in a long-distance migrant is constrained by the timing of its migratory journey. For long-distance migrants climate change may advance the phenology of their breeding areas, but the timing of some species' spring migration relies on endogenous rhythms that are not affected by climate change(8). Thus, the spring migration of these species will not advance even though they need to arrive earlier on their breeding grounds to breed at the appropriate time. We show that the migratory pied flycatcher Ficedula hypoleuca has advanced its laying date over the past 20 years. This temporal shift has been insufficient, however, as indicated by increased selection for earlier breeding over the same period. The shift is hampered by its spring arrival date, which has not advanced. Some of the numerous long-distance migrants will suffer from climate change, because either their migration strategy is unaffected by climate change, or the climate in breeding and wintering areas are changing at different speeds, preventing adequate adaptation. [KEYWORDS: Egg-laying trends; reproduction; temperature; population phenology; earlier; britain; tits]
    https://doi.org/10.1038/35077063
  • Proceedings of the Royal Society B-Biological Sciences
    2001

    The costs of egg production and incubation in great tits (Parus major)

    Marcel E. Visser, Kate Lessells
    The costs of egg production and incubation may have a crucial effect on avian reproductive decisions, such as clutch size and the timing of reproduction. We carried out a brood-size enlargement experiment on the great tit (Parus major), in which the birds had to lay and incubate extra eggs (full costs), only incubate extra eggs (free eggs) or did not pay an) extra cost (free chicks) in obtaining a larger brood. We used female fitness (half the recruits produced plus female survival) as a fitness measure because it is the female which pays the costs of egg production and incubation, and because clutch size is under female control. Female fitness decreased with increasing costs (fitness of free chicks females is higher than that of free eggs females which is higher than that of full costs females). These fitness differences were due to differences in female survival rather than in the number of recruits produced. This is the first time that the costs of egg production and incubation have been estimated using such a complete fitness measure, including, as our measure does, the local survival to the following year of both the female and her offspring. Our results emphasize that reproductive decisions cannot be understood without taking egg production and incubation costs into account. [KEYWORDS: fitness costs; clutch size; Parus major; egg production; incubation; climate change Flycatcher ficedula-albicollis; avian clutch size; energy-expenditure; parental effort; barn swallows; brood size; birds; reproduction; manipulation; constraints]
    https://doi.org/10.1098/rspb.2001.1661
  • Ecology
    2000

    Adaptive density dependence of avian clutch size

    Christiaan Both, J.M. Tinbergen, Marcel E. Visser
    In birds, the annual mean clutch size is often negatively correlated with population density. This relationship is at least in part due to adjustment by individuals. We investigated whether this response is adaptive in two ways. First we used an optimality model to predict how optimal clutch size (the clutch size that maximizes the number of breeding birds [recruits and surviving parents] in the next season) varies with density. We parameterized the model using data on fitness consequences of experimental variation in brood size and natural variation in population density in a Great Tit (Parus major) population. Predicted optimal clutch size decreased with density, but the predicted relationship was stronger than the observed relationship. Second, we investigated the relationship between the annual selection differential for clutch size and density. We found no relationship, indicating that there is no selection for a steeper than observed relationship between clutch size and density. This implies that the observed response is adaptive, and that the prediction of the optimality model lacks some important constraints or selection pressures. We further used the optimality model to examine the sensitivity of the optimal clutch size to density at different stages in the reproductive cycle. This analysis suggested that the nestling stage was most important. To the best of our knowledge this is the first study that makes quantitative predictions of optimal dutch size in relation to population density. [KEYWORDS: adaptation; clutch size; brood size manipulation; clutch size; density dependence; fitness; optimality model; Parus major; reaction norm Tit parus-major; brood-manipulation experiments; great tits; individual optimization; habitat heterogeneity; reproductive success; territory quality; offspring fitness; egg-production; birds]
    https://doi.org/10.1890/0012-9658(2000)081[3391:ADDOAC]2.0.CO;2
  • Journal of Animal Ecology
    2000

    Breeding territory size affects fitness: an experimental study on competition at the individual level

    Christiaan Both, Marcel E. Visser
    1. Descriptive studies have shown that the annual mean fecundity and survival in bird populations decline as density increases. Experimental studies in which breeding density has been manipulated show that density causally affects reproduction in some but not other species. 2. In a 3-year study on great tits Parus major we manipulated density by removing about one-third of territorial great tit pairs from half the study area each year. The removal resulted in an increase in territory size of the remaining birds in the experimental sub-area. 3. Fecundity and survival did not differ between the experimental low-density and the control sub-areas. The experiment thus did not show a causal relationship between breeding density and fecundity and survival at the level of the population. 4. The data were analysed further with respect to individual territory size, the level at which competition is assumed to operate. Pairs in the experimental sub-area enlarged their territories. We argue that variation in territory enlargement is not caused by individual quality. 5. Both pre- manipulation territory size and territory enlargement positively affected the probability that a territorial pair nested, the growth rate of their chicks, the number of fledglings that recruited into the breeding population and the survival of the territorial adults. No effect of territory enlargement was observed on clutch size, nor on the probability that pairs started a second brood. 6. The positive effect of the experimental territory enlargement argues for a causal effect of territory size on these reproductive parameters, independent of individual quality. 7. An effect of the density reduction on fecundity may not be detectable at the population level, either due to the large variation in territory sizes within the experimental treatments or to the negative effect of the experiment per sc, which counter balances the positive effect of territory enlargement. [KEYWORDS: brood size manipulation; density dependence; fitness; Parus major; removal experiment Tits parus-major; clutch size; great tits; density-dependence; habitat heterogeneity; ficedula-hypoleuca; offspring fitness; survival; reproduction; behavior]
    https://doi.org/10.1046/j.1365-2656.2000.00458.x
  • Ardea
    2000

    Great Tit Parus major survival, and the beech-crop cycle

    A.C. Perdeck, Marcel E. Visser, J.H. Van Balen
    The single most important environmental variable correlating with annual survival of both juvenile and adult Great Tits Parus major is the beech crop index (BCI). This index is a measure for the amount of seeds of beeches present in the winter, and correlates with crop size of several other tree species. Two, not mutually exclusive, hypotheses exist to explain the correlation between BCI and annual survival. The first is that the amount of seeds directly affects survival (winter-food limitation hypothesis). To test this hypothesis we re-analysed a supplemental food experiment of Van Balen (1980), extended with three more years of previously unpublished data. We found that supplemental food increased survival of both juveniles and adults, mainly in low BCI years, confirming the winter-food limitation hypothesis. The second hypothesis states that winters with a high BCI are preceded by springs with high densities of caterpillars (the breeding-season food limitation hypothesis). Using data of three long term studies of Dutch Great Tit populations we show that this hypothesis does not hold because (1) high BCI winters are not preceded by springs with high caterpillar densities, (2) annual mean juvenile fledging mass increased with increasing caterpillar densities, but no effect on parental mass was found, and (3) the annual survival of juveniles was not affected by the annual mean fledging mass, nor was annual adult survival affected by their mean mass during chick rearing. Finally we show that, despite the fact that the level of BCI probably can be predicted at the time of the breeding season and that both juvenile and adult survival is affected by BCI, reproductive decisions (clutch size, laying date and percentage second broods) are not affected by the BCI levels in the following winter. [KEYWORDS: Parus major; food limitation; food provisioning; population dynamics; survival Winter; population; food; fluctuations; density]
  • Ecography
    2000

    Consequences of dispersal for the quantitative study of adaptation in small-scale plots: a case study of an avian island population

    M.M. Lambrechts, Marcel E. Visser, N. Verboven
    Lifetime recruitment of breeding offspring estimated in small- scale study plots (i.e local recruitment) is considered to be the best available ecological measure of contributions to following generations, and sufficient for the quantitative study of adaptation in natural populations. Recent investigations suggest that local recruitment of breeding offspring does not always reflect the total recruitment in the whole population, especially in small-scale plots where the majority of locally-born offspring leave these plots to breed elsewhere. We examined in an avian island population whether study plot size has an important impact on different population and fitness measures. We defined around a central nestbox seven plots, varying in radius from 100 to 700 m. We show that in the smallest plots, the local replacement rate of adults by breeding offspring is low, the number of locally-born offspring settling beyond the limits of a plot is high, and relationships between local and total recruitment are weak. This is especially true for daughters as more daughters than sons settle beyond the limits of local plots for breeding. Our interpretation is that the lifetime recruitment of breeding offspring in local plots does not. necessarily reflect the lifetime recruitment of breeding offspring in the whole population, especially when plots do not cover the natal dispersal distance. Consequences of dispersal for the quantitative study of adaptation are discussed. [KEYWORDS: Great-tit; natal dispersal; environment; recruitment]
    https://doi.org/10.1034/j.1600-0587.2000.230502.x
  • Journal of Animal Ecology
    1999

    Interference among insect parasitoids: a multi-patch experiment

    Marcel E. Visser, T.H. Jones, G. Driessen
    1. Interference among insect parasitoids leads to a reduction in the overall search rate (the population equivalent of searching efficiency) with increasing parasitoid population density. When this reduction is due to behavioural responses of individuals to increased intraspecific competition, interference can serve as a stepping stone fron individual behaviour to population phenomena. 2. Interference can take different forms: (1) a direct within-patch reduction of searching efficiency with parasitoid density (direct mutual interference): (2) a decrease in overall search rate with increasing parasitoid density if parasitoids have a non-uniform distribution over patches where this distribution remains unaltered with increasing density (pseudo-interference); (3a) a decrease in the time spent on patches by each individual. i.e. more or longer travelling at higher parasitoid densities; and (3b) a decrease in overall search rate due to a change in the distribution of parasitoid effort over patches with Increasing parasitoid density. These last two forms arise from behavioural responses to increased parasitoid density and are forms of indirect mutual interference. 3. We present an expression for the overall search rate in a patchy environment where individual parasitoids travel between patches. We use this to show how the different forms of interference affect the overall search rate, contrasting environments with aggregated and uniform host distributions. 4. Using the data of Jones (1986) we explore the different forms of interference in a multipatch experiment. In these experiments, different numbers of parasitoids were introduced in an arena where the distribution of hosts over patches was either aggregated or uniform. We show that both pseudo-interference and indirect mutual interference play a role, and that they have an opposite effect for a uniform host distribution, but amplify one another for aggregated host distributions. 5. The indirect mutual interference arises from a shift towards a more uniform distribution of parasitoid effort over patches with increasing parasitoid densities. This shift is caused by a behavioural response to parasitoid density, and is likely due to changes in the parasitoids' patch arrival and departure decisions. These decisions underlie the distribution of time spent on patches, thereby linking individual behaviour to a phenomenon at the population level. 6. Finally, we put forward a more general framework for indirect mutual interference to also include behavioural responses in sex allocation, clutch size and host acceptance to parasitoid density as forms of interference. [KEYWORDS: interference; overall search rate; parasitoid; population dynamics; searching efficiency; Trybliographa rapae Ideal free distribution; clutch size; adaptive uperparasitism; drosophila parasitoids; solitary parasitoids; mutual interference; venturia-canescens; time allocation; sex-ratio; patterns]
    https://doi.org/10.1046/j.1365-2656.1999.00269.x
  • Proceedings of the Royal Society B-Biological Sciences
    1999

    Density-dependent recruitment rates in great tits: the importance of being heavier

    Christiaan Both, Marcel E. Visser, N. Verboven
    In birds, individuals with a higher mass at fledging have a higher probability of recruiting into the breeding population. This can be because mass is an indicator of general condition and thereby of the ability to survive adverse circumstances, and/or because fledging mass is positively related to competitive strength in interactions with other fledglings. This latter explanation leads to two testable predictions: (i) there is stronger selection for fledging mass when there is more severe competition (i.e. at higher densities); and (ii) that besides absolute hedging mass, relative mass of fledglings within a cohort is important. We test these two predictions in two great tit (Parus major) populations. The first prediction was met for one of the populations, showing that competition affects the importance of mass-dependent recruitment. The second prediction, that fledglings recruit relatively well if they are heavy compared to the other fledglings, is met for both populations. The consequence of the importance of relative rather than absolute fledging mass is that the fitness consequences of reproductive decisions affecting fledging mass, such as clutch size, depend on the decisions of other individuals in the population. [KEYWORDS: Parus major; density dependence; selection; body mass; fledging mass; recruitment Parus-major; clutch size; juvenile survival; nestling weight; song sparrows; population; dominance; selection]
    https://doi.org/10.1098/rspb.1999.0660
  • Oikos
    1999

    Long-term fitness effects of fledging date in great tits

    Marcel E. Visser, N. Verboven
    Reproductive decisions, such as timing of reproduction and the number of offspring to product, affect the conditions for the offspring at the time of independence These conditions can refer to the state of an individual, such as mass, or of the environment, such as time of the season, and will affect the reproductive value of the offspring. Knowledge of these fitness consequences is important when assessing the adaptive value of reproductive decisions. However it is often unclear how long- term the effect of these conditions is on an individual's reproductive success. Previous work has shown that the probability thar great tit fledglings recruit into the breeding population is strongly affected by their fledging date and mass. Using a long-term field study of a great tit population, we studied whether fledging conditions (fledging date, fledging mass and tarsus length) also affected reproductive success after an individual had recruited into the breeding population. For female recruits. this was not the case. For males, however, there was an effect of fledging date on lifetime reproductive success (LRS), calculated for individuals that had recruited. Males that fledged late produced fer er recruiting offspring in their first year of breeding partly because they had a twice as high probability that their breeding attempt failed to produce fledglings. Due to this decrease in LRS of recruited sons with increase in their hedging date, the fitness cost of breeding late is underestimated when counting the number of recruits produced from a breeding attempt. [KEYWORDS: Parus-major; clutch size; establishment; reproduction; dispersal; dominance; palustris]
    https://doi.org/10.2307/3546694
  • Oikos
    1998

    Seasonal variation in local recruitment of great tits: the importance of being early

    N. Verboven, Marcel E. Visser
    To understand seasonal variation in reproductive decisions it is important to quantify the fitness costs and benefits of these decisions in relation to date within breeding season. In this paper we investigate the effect of hedging date on local recruitment of great tits (Parus major). The probability that fledglings were recaptured as breeding birds was analysed in long-term data sets of two great tit populations in the Netherlands, one on the mainland (Hoge Veluwe) and one on an island (Vlieland). The results showed that young that fledged early in the breeding season were more likely to recruit into the breeding population than young that fledged late. The negative relationship between local recruitment and fledging date was also present after controlling for fledging mass, year, sex and brood type (first, replacement or second brood). Moreover, the relationship did not seem to be due to late hedged young being more likely to disperse. The decline of local recruitment rate with hedging date was Further tested with two experiments. In the first experiment clutches were removed, forcing parents to lay a replacement clutch and thereby delaying the hedging date of their young. Fledglings from experimental pairs had significantly lower recruitment rates than fledglings from unmanipulated controls, showing that local recruitment was causally related to hedging date. In the second experiment fledging date was not changed, but the parents and the territory from which the young fledged were altered by swapping clutches between parents with early and]ale laying dates. No significant differences were found in recruitment rates of fledglings between the treatments and unmanipulated controls. There was no evidence for an indirect relationship between recruitment and fledging dale through different quality fledglings produced by early and late parents. One of the reasons for the observed seasonal variation in reproductive decisions is that early and]ate fledglings do not contribute equally to the parents' fitness. [KEYWORDS: Guillemots uria-aalge; parus-major; reproductive success; winter survival; causal relationship; juvenile survival; fledging success; breeding success; natal dispersal; nestling weight]
    https://doi.org/10.2307/3546771
  • Biological Control
    1998

    The influence of competition between foragers on clutch size decisions in insect parasitoids

    Marcel E. Visser, J.A. Rosenheim
    The effect of competition between ovipositing females on their clutch size decisions is studied in parasitoid insects. The effect of this competition depends on whether the competition between parasitoid larvae within a host is contest (solitary parasitoids) or scramble competition (gregarious parasitoids). For gregarious parasitoids, a decreasing clutch size with increasing competition between females is predicted while for solitary parasitoids an increase is predicted. These predictions mere tested using the gregarious parasitoid Aphaereta minuta (M. E. Visser, 1996, Behav. Ecol. 7, 109-114) and the solitary parasitoid Comperiella bifasciata (J. A. Rosenheim and D. Hongkham, 1996, Anim. Behav. 51, 841-852). Parasitoids were either kept alone or in groups before the experiments, in which they were introduced singly into a patch containing unparasitized hosts. In the experiment with A. minuta, females kept together before the experiment laid smaller clutches than females kept alone. In C. bifasciata, the clutch size laid by females kept together was larger than that of females kept alone. Thus, both predictions were supported. [KEYWORDS: parasitoids; clutch size; competition; Aphaereta minuta; Comperiella bifasciata Hymenoptera; superparasitism; patch; oviposition; braconidae; allocation; females; wasp]
    https://doi.org/10.1006/bcon.1997.0589
  • Proceedings of the Royal Society B-Biological Sciences
    1998

    Warmer springs lead to mistimed reproduction in great tits (Parus major)

    Marcel E. Visser, Arie Van Noordwijk, J.M. Tinbergen, Kate Lessells
    In seasonal environments, the main selection pressure on the timing of reproduction (the ultimate factor) is synchrony between offspring requirements and food availability. However, reproduction is initiated much earlier than the time of maximum food requirement of the offspring. Individuals should therefore start reproduction in response to cues (the proximate factors), available in the environment of reproductive decision making, which predict the later environment of selection. With increasing spring temperatures over the past decades, vegetation phenology has advanced, with a concomitant advancement in the reproduction of some species at higher trophic levels. However, a mismatch between food abundance and offspring needs may occur if changes in the environment of decision making do not match those in the environment of selection. Date of egg laying in a great tit (Parus major) population has not advanced over a 23-year period, but selection for early laying has intensified. We believe that this is the first documented case of an adaptive response being hampered because a changing abiotic factor affects the environment in which a reproductive decision is made differently from the environment in which selection occurs. [KEYWORDS: timing of reproduction; laying date; Parus major; phenotypic plasticity; climate change; selection Winter moth; selection; growth; birds]
    https://doi.org/10.1098/rspb.1998.0514
  • Behavioral Ecology
    1996

    The influence of competition between foragers on clutch size decisions in an insect parasitoid with scramble larval competition

    The effect of competition between ovipositing females on their clutch size decisions is studied in animals that lay their eggs in discrete units of larval food (hosts). In such species the effect of competition depends on the form of the larval competition within such units. In insect parasitoids, there might either be contest (solitary parasitoids) or scramble competition (gregarious parasitoids) between larvae within a host. For gregarious parasitoids, a decreasing clutch size with increasing competition between foragers is predicted. This prediction is tested in experiments using the parasitoid Aphaereta minuta. Parasitoids were either kept alone or in groups of four before the experiment, in which they were introduced singly in a patch containing unparasitized hosts. Animals kept together laid on average clutches of 0.74 eggs smaller than females kept alone (average clutch is 5.3), thereby confirming the prediction. Clutch size decreased with encounter number, which might be due to the adjustment of the female's estimate of the encounter rate with hosts. Finally, the results are compared with those reported for solitary parasitoids (that have scramble larval competition), for which it is predicted that the clutch size will increase with increasing levels of competition between females. [KEYWORDS: competition, clutch size, parasitoids, super parasitism]
    https://doi.org/10.1093/beheco/7.1.109
  • Animal Behaviour
    1995

    The effect of competition on oviposition decisions of Leptopilina heterotoma (Hymenoptera: Eucoilidae)

    Prey selection models in which a patch is depleted by a number of foragers predict that the less profitable prey are rejected early in the foraging bout, but accepted later on. Such behaviour would lead to partial preferences: certain prey types are sometimes rejected and sometimes accepted (eaten), even within the same foraging bout. In the absence of competition, however, parasitoids should show no such switch in behaviour. This prediction was tested using the insect parasitoid Leptopilina heterotoma (Hymenoptera: Eucoilidae) searching a patch containing unparasitized and parasitized (less profitable) hosts. In the experiments, the degree of competition was varied by (1) having either a single parasitoid or two parasitoids simultaneously searching on the patch, and (2) keeping parasitoids either alone or together with conspecifics before the experiment. For a given patch quality (expressed as the average quality of the five previously encountered hosts), parasitoids accepted parasitized hosts more often when they searched a patch alone than when there were competitors present. Competition clearly influenced oviposition decisions. The predicted switch in behaviour was observed in the presence of competition, and a much less pronounced change in the absence of it. Keeping parasitoids alone or together before the experiment did influence the oviposition decisions but in the opposite way to that predicted: the latter accepted parasitized hosts more readily at high patch quality than the former. Finally, it was shown that the parasitoids are able to distinguish between the four types of host (unparasitized, once parasitized by a conspecific, once parasitized by the female herself and twice parasitized). [KEYWORDS: PATCH TIME ALLOCATION, ADAPTIVE SUPERPARASITISM, SOLITARY PARASITOIDS, ESS MODEL, SELECTION, DIET, INFORMATION, EXPERIENCE, CYNIP, HOSTS]
    https://doi.org/10.1016/0003-3472(95)90089-6

Projecten & samenwerkingen

Projecten

Outreach

Categories