Projects

Causes and consequences of variation in the migratory phenotype in a long-lived seabird (part of SFB1372)

Understanding the evolutionary potential and trajectories of migratory behaviour requires detailed knowledge of the patterns, sources, and consequences of variance in the migratory phenotype. Ideally, one would partition this variance into its underlying components, and learn which parts are underpinned by a genetic basis, which parts result from parental or other natal effects, and which parts are shaped by previously or currently experienced environmental conditions. In a next step, the variance in each of these parts could then be related to variance in fitness, to learn how selection acts on migratory behaviour and whether any response to selection can be expected.

Using light-level geolocators (Kürten et al. 2019), we have so far collected 284 tracks of migratory journeys performed by 140 Banter See common terns, breeding in our long-term study population located at the Banter See (Kürten et al. 2022). Since almost all of these birds are of known sex, age and ancestry and since detailed information on their natal conditions, as well as annual local return, phenology and reproductive performance is available, assessing the causes and consequences of variance in their migratory phenotype is now within reach.

Publications

Wynn J, Kürten N, Moiron M, Bouwhuis S (2025) Selective disappearance based on navigational efficiency in a long-lived seabird. Journal of Animal Ecology 94: 535-544 

Kürten N, Wynn J, Haest B, Schmaljohann H, Vedder O, González-Solís J, Bouwhuis S (2025) Route flexibility is associated with headwind minimization in a long-distance migratory seabird. Proceedings of the Royal Society B 292: 20242522

Bertram J, Kürten N, Bichet C, Schupp PJ, Bouwhuis S (2022) Mercury contamination level is repeatable and predicted by wintering area in a long-distance migratory seabird. Environmental Pollution 313: 120107

Kürten N, Schmaljohann H, Bichet C, Haest B, Vedder O, González-Solís J, Bouwhuis S (2022) High individual repeatability of the migratory behaviour of a long-distance migratory seabird. Movement Ecology 10: 5

Kürten N, Vedder O, González-Solís J, Schmaljohann H, Bouwhuis S (2019) No detectable effect of light-level geolocators on the behaviour and fitness of a long-distance migratory seabird. Journal of Ornithology 160: 1087-1095

Causes and consequences of mercury pollution

Industrial activities and other drivers of global change, such as ongoing climate warming, increase environmental mercury levels. As mercury enters aquatic ecosystems, microorganisms transform it into its organic and bioavailable form, methylmercury. When biota ingest methylmercury, it can accumulate along the food chain, exposing long-lived top predators, such as some seabird species, to particularly high levels.

We study the causes and consequences of mercury pollution in the Banter See common terns. Hereto, we collect (i) blood samples from incubating birds (e.g. 1314 samples from 588 birds between 2017 and 2023) using ‘kissing bugs’ specifically bred for this purpose (Becker et al. 2006), as well as (ii) feather samples from birds that were tracked with geolocators or that died of avian influenza (e.g. 1560 samples from 316 birds between 2017 and 2023) and (iii) samples of food items brought into the breeding colony. These samples are analyzed to quantify mercury contamination levels, in order to investigate how variation in mercury levels is explained by (i) migratory behaviour (Bertram et al. 2022), (ii) sex, phenology and within-individual accumulation with age (Bertram et al. 2024a), and (iii) genetic disposition (Bertram et al. 2024b), as well as (iv) its transfer across generations (Bertram et al. 2025a, Bertram et al. 2025b) and (v) its potential effects on the immune system and long-term fitness consequences.

In addition, we study mercury contamination in the non-piscivorous gull-billed tern as well (Schnelle et al. 2025), and causality of the observed patterns is being established with experiments on captive Japanese quail.

Publications

Bertram J, Bichet C, Moiron M, Beccardi M, Kürten N, Schupp PJ, Bouwhuis S (2025b) Mercury levels in chicks of a long-lived seabird – parental effects and links with growth and survival. Environmental Research 285: 122283

Bertram J, Kürten N, Bichet C, Moiron M, Schupp PJ, Bouwhuis S (2025a) Parental blood mercury levels are correlated, and predictive of those in eggs in a long-lived seabird. Environmental Research 275: 121437

Bertram J, Moiron M, Bichet C, Kürten N, Schupp PJ, Bouwhuis S (2024b) Mercury concentrations in blood and back feathers are repeatable, heritable and correlated in a long-lived seabird. Science of the Total Environment 955: 176939 

Bertram J, Bichet C, Moiron M, Schupp PJ, Bouwhuis S (2024a) Sex- and age-specific mercury accumulation in a long-lived seabird. Science of the Total Environment 927: 172330

Bertram J, Kürten N, Bichet C, Schupp PJ, Bouwhuis S (2022) Mercury contamination level is repeatable and predicted by wintering area in a long-distance migratory seabird. Environmental Pollution 313: 120107

Schnelle A, Risch M, Schupp PJ, Liedvogel M*, Bouwhuis S* (2025) Sex- and age-specific mercury contamination in Central Europe’s last gull-billed tern population. Environmental Pollution 374: 126264 (*shared senior authorship)

Effects of avian influenza on two tern species

The anthropogenic influence on wildlife hardly knows any boundary. We cause habitat loss and climate change, deplete natural resources and emit pollutants. In addition, we create ideal environments for the emergence of novel pathogens, such as a strain of highly pathogenic avian influenza virus that originated in poultry farming in the 1990s: H5N1. Seabirds are among the birds most affected by these changes and during the breeding seasons of 2022 and 2023 were introduced to unprecedented H5N1 outbreaks at their breeding sites. The long-term study population of common terns at the Banter See suffered immense losses of breeding adults, as well as their chicks, causing a population crash. Thanks to the long-term nature of our study, including access to archived blood and plasma samples, we are in the perfect position to (i) investigate which factors caused birds at this colony to die of avian influenza (e.g. sex, age, phenology, genetic variation at immunity genes, levels of mercury pollution), as well as (ii) to study the development and maintenance of antibodies against avian influenza.

To compare antibody development across populations and species, we have also started sampling common terns, as well as gull-billed terns making up the last Central-European breeding population, at Neufelderkoog.

Publications

Ewing DA, Bouwhuis S (in press) Estimating epidemiological parameters of highly pathogenic avian influenza in common terns using exact Bayesian inference. Journal of Animal Ecology

Pohlmann A, Stejskal O, King J, Bouwhuis S, Packmor F, Ballstaedt E, Hälterlein B, Hennig V, Stacker L, Graaf A, Hennig C, Günther A, Liang Y, Hjulsager C, Beer M, Harder T (2023) Mass mortality among colony-breeding seabirds in the German Wadden Sea in 2022 due to distinct genotypes of HPAIV H5N1 clade 2.3.4.4b. Journal of General Virology 104: 001834

Popular science contributions (in German)

Bouwhuis S (2024) Flussseeschwalbe trifft Vogelgrippe – erste Erkenntnisse aus einer Langzeitstudie. „Natur- und Umweltschutz“ Zeitschrift der Naturschutz und Forschungsgemeinschaft Der Mellumrat e.V. 23, 24-27. ISSN: 1619-8565

Bouwhuis S (2023) Flussseeschwalbe trifft Vogelgrippe – die traurige Geschichte des Jahres 2022. Nachrichten des Marschenrates zur Förderung der Forschung im Küstengebiet der Nordsee 60, 61-68. ISSN: 0931-5373 

Nature vs. nurture in common terns – a variance partitioning approach

Phenotypic variation in wild populations is generally the result of many genes with small effects (additive genetic variance), that often act in combination with individual variation introduced during development (permanent individual variance), and environmental effects such as abiotic or biotic factors (environmental variance). By applying a statistical model based on a variance-partitioning approach, quantitative genetics allows to estimate the levels of additive genetic variance, its magnitude relative to the overall phenotypic variance (the so-called the trait’s heritability), as well as the correlation structure between heritable traits. The latter is important for understanding the evolutionary trajectories of traits, because only when a trait is genetically correlated with fitness can it evolve through natural selection.

Using the information of social parents and their offspring, we can construct a social pedigree of the Banter See common terns. This pedigree is a good approximation of the genetic pedigree, because common terns exhibit very low levels of extra-pair paternity (González-Solís et al. 2001), and for the period 1992-2023, it comprises 10,581 records, covers 7 generations, and contains 912 and 798 paternities and maternities, respectively. As such, it offers the possibility of effectively studying the quantitative genetics of traits such as laying date (Moiron et al. 2020), telomere length (Vedder et al. 2022), fitness (Moiron et al. 2022), arrival date (Moiron et al. 2024), social ageing (Moiron & Bouwhuis 2024) and mercury contamination (Bertram et al. 2024).

Publications

Bertram J, Moiron M, Bichet C, Kürten N, Schupp PJ, Bouwhuis S (2024) Mercury concentrations in blood and back feathers are repeatable, heritable and correlated in a long-lived seabird. Science of the Total Environment 955: 176939 

Moiron M, Bouwhuis S (2024) Age-dependent shaping of the social environment in a long-lived seabird – a quantitative genetic approach. Philosophical Transactions B 379: 20220465

Moiron M, Teplitsky C, Haest B, Charmantier A*, Bouwhuis S* (2024) Micro-evolutionary response of spring migration timing in a wild seabird. Evolution Letters 8: 8-17 (*shared senior authorship)

Moiron M, Charmantier AC*, Bouwhuis S* (2022) The quantitative genetics of fitness in a wild seabird. Evolution 76: 1443-1452 (*shared senior authorship)

Vedder O, Moiron M, Bichet C, Bauch C, Verhulst S, Becker PH, Bouwhuis S (2022) Telomere length is heritable and genetically correlated with lifespan in a wild bird. Molecular Ecology 31: 6297-6307

Moiron M, Araya-Ajoy YG, Teplitsky C, Bouwhuis S*, Charmantier A* (2020) Understanding the social dynamics of breeding phenology: indirect genetic effects and assortative mating in a long distance migrant. American Naturalist 196: 566-576 (*shared senior authorship)

González-Solís J, Sokolov E, Becker PH (2001) Courtship feedings, copulations and paternity in common terns, Sterna hirundo. Animal Behaviour 61: 1125-1132

Protection of the last gull-billed tern population in Central Europe

The gull-billed tern (Gelochelidon nilotica) is a medium-sized tern whose last colony in Central Europe is located in the Elbe estuary of Dithmarschen (state of Schleswig-Holstein). By 2010, this population had shrunk to 41 breeding pairs, which led the state of Schleswig-Holstein to take responsibility for its preservation by founding a "Species conservation project for the gull-billed tern" in 2011, administrated by the ‘Bündnis Naturschutz in Dithmarschen e.V.’. The aim of the project is to prevent the extinction of the population and to ensure the protection of the large multi-species colony consisting of three species of terns, black-headed gulls, avocets, oystercatchers and other ground-nesting birds. Fencing to minimise mammalian predation pressure and habitat management currently are the main methods employed. 

In 2021, we teamed up with the members of the conservation project to investigate the extent to which potential threats other than predation or habitat structure, such as food shortage (Schnelle et al. 2024a), limited genetic diversity (Schnelle et al. 2024b) or pollution (Schnelle et al. 2025a, Schnelle et al. 2025b) could limit the growth of the population. After the outbreak of avian influenza in the breeding seasons of 2022 and 2023, we additionally started monitoring the development of antibodies against this viral disease in both the gull-billed terns and one of their host species, the common tern. Future work would benefit from extending our information about these birds beyond the breeding season or establishing further suitable breeding habitat to mitigate the risk associated with the population being in a single location.

Publications

Schnelle A, Peter M, Müller C, Risch M, Liedvogel M*, Bouwhuis S* (2025b) A comprehensive assessment of contaminant exposure in an endangered tern population. Environmental Research 285: 122444 (*shared senior authorship)

Schnelle A, Risch M, Schupp PJ, Liedvogel M*, Sandra Bouwhuis* (2025a) Sex- and age-specific mercury contamination in Central Europe’s last gull-billed tern population. Environmental Pollution 374: 126264 (*shared senior authorship)

Schnelle A, Rollins RE, Cecere JG, Sánchez Gutiérrez J, Masero JA, Risch M, Bouwhuis S*, Liedvogel M* (2024b) Assessment of genetic diversity in a locally endangered tern species suggests population connection instead of isolation. Conservation genetics (*shared senior authorship)

Schnelle A, Winter M, Bouwhuis S, Risch M (2024a) Diet composition and reproductive performance in Central Europe’s last gull-billed tern population - a long term study. Ardea 112: 247-258 

Ageing common terns

Knowledge of a species’ age-specific pattern of survival and reproduction is fundamental to understanding its life history evolution and population dynamics. We investigated the age-specificity of various traits in the Banter See common terns. We found that while survival probability monotonously declined with age (Zhang et al. 2015a), various phenological and reproductive traits gradually improved with age, before levelling off (Zhang et al. 2015b). These age-related improvements were mostly due to within-individual changes in trait expression, and while effects of selective appearance and disappearance provided evidence for quality differences between individuals, these effects were small (Zhang et al 2015b). Correcting for changes in trait expression with age, we found within-individual variation in phenology and reproductive success to be associated with mortality risk (Zhang et al. 2015c). Specifically, we found that if individual birds arrived and bred earlier than they did on average and laid larger clutches and eggs than they did on average, their mortality risk increased. We therefore showed that when quality differences between birds (Vedder & Bouwhuis 2018) are accounted for, survival costs of early and successful reproduction can be observed (also see Vedder et al. 2021). Finally, we combined performance measures to calculate age-specific reproductive values, and found evidence for senescence (Zhang et al. 2015a). The fitness cost of this senescence was, at ~20%, slightly higher than reported for other bird species (Bouwhuis & Vedder 2017).

Across generations, we found ageing parents to produce more male- than female-biased broods, as well as sex-specific pathways of parental age effects on offspring lifetime reproductive success: recruited sons from older fathers suffer from a reduced lifespan, while recruited daughters from older mothers suffer from reduced reproductive performance throughout life (Bouwhuis et al. 2015). The latter effect may (partly) be explained by daughters from older mothers fledging with a reduced body mass and remaining a low body mass throughout life (Bouwhuis et al. 2015), a pattern that itself cannot be explained by sex- and age-specific parental provisioning behaviour (Cansse et al. 2024).

Publications

Moiron M, Bouwhuis S (2024) Age-dependent shaping of the social environment in a long-lived seabird – a quantitative genetic approach. Philosophical Transactions B 379: 20220465 

Cansse T, Vedder O, Kürten N, Bouwhuis S (2024) Feeding rate reflects quality in both parents and offspring: a longitudinal study in common terns. Animal Behaviour 214: 111-120

Vedder O, Pen I, Bouwhuis S (2021) How fitness consequences of early-life conditions vary with age in a long-lived seabird: a Bayesian multivariate analysis of age-specific reproductive values. Journal of Animal Ecology 90: 1505-1514

Vedder O, Bouwhuis S (2018) Heterogeneity in individual quality in birds: overall patterns and insights from a study on common terns. Oikos 127: 719-727

Bouwhuis S, Vedder O (2017) Avian escape artists? Patterns, processes and costs of senescence in wild birds. In: The evolution of senescence in the tree of life. Eds. Shefferson RP, Jones OR, Salguero-Gómez R. Cambridge University Press, Cambridge (UK)

Vedder O, Bouwhuis S, Benito MM, Becker PH (2016) Male-biased sex allocation in ageing parents; a longitudinal study in a long-lived seabird. Biology Letters 12: 20160260

Bouwhuis S, Vedder O, Becker PH (2015) Sex-specific pathways of parental age effects on offspring lifetime reproductive success in a long-lived seabird. Evolution 69: 1760-1771

Zhang H, Vedder O, Becker PH, Bouwhuis S (2015c) Contrasting between- and within-individual trait effects on mortality risk in a long-lived seabird. Ecology 96: 71-79

Zhang H, Vedder O, Becker PH, Bouwhuis S (2015b) Age-dependent trait variation: the relative contribution of within-individual change, selective appearance and disappearance in a long-lived seabird. Journal of Animal Ecology 84: 797-807

Zhang H, Rebke M, Becker PH, Bouwhuis S (2015a) Fitness prospects: effects of age, sex and recruitment age on reproductive value in a long-lived seabird. Journal of Animal Ecology 84: 199-207

Epigenetic underpinnings of ageing in common terns?

Parental age is one aspect of the parental phenotype known to have consequences for aspects of offspring phenotype and fitness. Offspring from old parents have, for example, been found to have a reduced probability to recruit to the breeding population (e.g. Bouwhuis et al. 2009) or an altered (e.g. Bouwhuis et al. 2010) or reduced annual reproductive success or lifespan (Bouwhuis et al. 2015) after recruitment. The inheritance of epigenetic alterations to gene expression is a potential mechanistic explanation underlying parental effects in general, and of specific interest especially for species in which negative parental age effects on offspring have been found, despite parental care improving with age due to increased experience (e.g. Limmer & Becker 2009) or older parents being better at chick provisioning in general (e.g. Cansse et al. 2024). 

We obtained repeated blood samples from 17 breeding pairs and their offspring. These samples have undergone reduced representation bisulfite sequencing (RRBS) to characterise genome-wide DNA methylation profiles on the single nucleotide level. In addition, we have sequenced, de novo assembled and annotated a reference genome for the common tern (Meyer et al. 2023). With these data, we will be able to answer the following questions:

* do adult DNA methylation patterns change with age within individual common terns and does any within-individual change in adult DNA methylation pattern depend on sex?

* do offspring DNA methylation patterns resemble those of (one of) their parent(s) and do (sex-specific) offspring DNA methylation patterns predict offspring development or survival?

Publications

Cansse T, Vedder O, Kürten N, Bouwhuis S (2024) Feeding rate reflects quality in both parents and offspring: a longitudinal study in common terns. Animal Behaviour 214: 111-120

Meyer B, Moiron M, Caswara C, Chow W, Fedrigo O, Formenti G, Haase B, Howe K, Mountcastle J, Uliano-Silva M, Wood J, Jarvis ED, Liedvogel M*, Bouwhuis S* (2023) Sex-specific changes in autosomal methylation rate in ageing common terns. Frontiers in Ecology and Evolution 11: 982443 (*shared senior authorship)

Bouwhuis S, Vedder O, Becker PH (2015) Sex-specific pathways of parental age effects on offspring lifetime reproductive success in a long-lived seabird. Evolution 69: 1760-1771

Bouwhuis S, Charmantier A, Verhulst S, Sheldon BC (2010) Individual variation in rates of senescence: natal origin effects and disposable soma in a wild bird population. Journal of Animal Ecology 79: 1251-1261

Limmer B, Becker PH (2009) Improvement in chick provisioning with parental experience in a seabird. Animal Behaviour 77: 1095e1101

Bouwhuis S, Sheldon BC, Verhulst S, Charmantier A (2009) Great tits growing old: selective disappearance and the partitioning of senescence to stages within the breeding cycle. Proceedings of the Royal Society B 276: 2769-2777

Common tern info center

Climate change and other human activities are causing profound effects on marine ecosystem productivity, with many seabirds showing alarming declines (Sydeman et al. 2021). Based on the idea that "…we will conserve only what we love, we will love only what we understand, and we will understand only what we are taught", we aimed to exchange our informal public tours to the common tern population at the Banter See for a proper exhibition allowing better views and larger group sizes, including school classes. In collaboration with the city of Wilhelmshaven, funded by the DBU and NBank, and making use of the artistic talents of Uwe Franzen and Dr Maria Röbbelen, we therefore designed and established an exhibition on our ‘Weltenbummler’. This exhibition opened on the 12th of May 2023 and is now managed by the UNESCO-Weltnaturerbe Wattenmeer Besucherzentrum Wilhelmshaven.

Publications

Sydeman WJ, Schoeman DS, Thompson SA, Hoover BA, García-Reyes M, Daunt F, Agnew P, Anker-Nilssen T, Barbraud C, Barrett R, Becker PH, Bell E, Boersma PD, Bouwhuis S, Cannell B, Crawford RJM, Dann P, Delord K, Elliott G, Erikstad KE, Flint E, Furness RW, Harris MP, Hatch S, Hilwig K, Hinke JT, Jahncke J, Mills JA, Reiertsen TK, Renner H, Sherley RB, Surman C, Taylor G, Thayer JA, Trathan PN, Velarde E, Walker K, Wanless S, Warzybok P, Watanuki Y (2021) Hemispheric asymmetry in ocean change and the productivity of marine ecosystem sentinels. Science 372: 980-983

A scientific approach to habitat restauration – the Augustgroden project

Us humans inhabiting the Wadden Sea region need dikes to protect us from the sea. These dikes, in turn, need clay for being maintained, leaving clay pits in the places where this clay has been obtained from. If we manage these clay pits wisely, they can turn into the perfect breeding, resting and feeding habitat for endangered sea-, meadow- and waterbirds. This way, protection of people and birds can go hand in hand – a beautiful thing!

Since 2024, Markus Risch and I are collaborating with the National Park of Lower Saxony and the Naturschutzstiftung FWW to restore breeding habitat for terns and other meadow- and waterbirds using a clay pit in Augustgroden. In March 2024, we teamed up with a large number of volunteers to prepare the islands in the clay pit for the birds. We spent various long weekends trimming back the vegetation and building electric fences to keep potential predators out. Trail cameras placed on site clearly showed that the birds were grateful and numerously appearing during the early season, even courtshipping in front of the cameras. The vegetation, however, showed more tenacity than we had imagined, and claimed back the islands. This taught us that we need to come better prepared, such that we are now working on various other solutions, adopting an experimental approach to see what the birds would prefer us to do for future breeding seasons.