Mo Verhoeven

Dr. Mo Verhoeven

Postdoc
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Visiting Address

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands

About

I'm an avian ecologist working in the ArcticMigrants project together with a large consortium of researchers.

Biography

- Drew Redshank in primary school
- Observed Lapwing in high school
- Studied Red Knots and Tree Swallows at university
- PhD on Black-tailed Godwits
- PostDoc on Arctic migratory birds

Research groups

CV

Employment

  • 2021–Present
    PostDoc at NIOO/NIOZ
  • 2019–2021
    PostDoc at the Royal Society for the Protection of Birds

Education

2015–2019
PhD

Editorial board memberships

  • 2020–Present
    Wader Study
  • 2020–Present
    Journal of Caribbean Ornithology

Publications

Peer-reviewed publications

  • Avian Research
    2023

    Predicting the non-breeding distributions of the two Asian subspecies of Black-tailed Godwit using morphological information

    Bing Run Zhu, Mo Verhoeven, Chris J. Hassell, Katherine K.S. Leung, Dmitry Dorofeev, Qiang Ma, Krairat Eiamampai, Jonathan T. Coleman, Uchrakhzaya Tserenbat, Gankhuyag Purev-Ochir, David Li, Zhengwang Zhang, Theunis Piersma

    Until recently, Limosa limosa melanuroides was thought to be the only subspecies of Black-tailed Godwit in the East Asian–Australasian Flyway. For this reason, all previous occurrences and counts of Black-tailed Godwits in the flyway have been assigned to melanuroides. However, a larger-bodied subspecies, bohaii, has recently been discovered in the flyway. As a result, the occurrence of Black-tailed Godwits in the flyway needs to be reconsidered such that the specific distribution of each subspecies becomes known. To this end, we developed a simple discriminant function to assign individuals to subspecies based on their bill and wing length. Cross-validation with individuals known to be bohaii or melanuroides, based on molecular analysis, showed the developed function to be 97.7% accurate. When applied to measurements of godwits captured at 22 sites across 9 countries in East–Southeast Asia and Australia, we found that bohaii and melanuroides occurred at most sites and overlapped in their distribution from Kamchatka to Australia. We examined photos from all along the flyway to verify this surprising result, confirming that both subspecies co-occur in most locations. Based on these results, we hypothesise that bohaii and melanuroides from the west of their breeding ranges mostly migrate over Chinese mainland. Birds of both subspecies from the east of their ranges are expected to migrate along the Pacific Ocean. We encourage ringing groups in East–Southeast Asia and Australia to use this simple method to keep adding knowledge about Black-tailed Godwits in the East Asian–Australasian Flyway.

    https://doi.org/10.1016/j.avrs.2022.100069
  • Journal of Animal Ecology
    03-2022

    Age-dependent timing and routes demonstrate developmental plasticity in a long-distance migratory bird

    Mo Verhoeven, A.H. Jelle Loonstra, Alice D. McBride, Wiebe Kaspersma, Jos C.E.W. Hooijmeijer, Christiaan Both, Nathan R Senner, Theunis Piersma

    Longitudinal tracking studies have revealed consistent differences in the migration patterns of individuals from the same populations. The sources or processes causing this individual variation are largely unresolved. As a result, it is mostly unknown how much, how fast and when animals can adjust their migrations to changing environments. We studied the ontogeny of migration in a long-distance migratory shorebird, the black-tailed godwit Limosa limosa limosa, a species known to exhibit marked individuality in the migratory routines of adults. By observing how and when these individual differences arise, we aimed to elucidate whether individual differences in migratory behaviour are inherited or emerge as a result of developmental plasticity. We simultaneously tracked juvenile and adult godwits from the same breeding area on their south- and northward migrations. To determine how and when individual differences begin to arise, we related juvenile migration routes, timing and mortality rates to hatch date and hatch year. Then, we compared adult and juvenile migration patterns to identify potential age-dependent differences. In juveniles, the timing of their first southward departure was related to hatch date. However, their subsequent migration routes, orientation, destination, migratory duration and likelihood of mortality were unrelated to the year or timing of migration, or their sex. Juveniles left the Netherlands after all tracked adults. They then flew non-stop to West Africa more often and incurred higher mortality rates than adults. Some juveniles also took routes and visited stopover sites far outside the well-documented adult migratory corridor. Such juveniles, however, were not more likely to die. We found that juveniles exhibited different migratory patterns than adults, but no evidence that these behaviours are under natural selection. We thus eliminate the possibility that the individual differences observed among adult godwits are present at hatch or during their first migration. This adds to the mounting evidence that animals possess the developmental plasticity to change their migration later in life in response to environmental conditions as those conditions are experienced.

    https://doi.org/10.1111/1365-2656.13641
  • Global Change Biology
    2022

    Current breeding distributions and predicted range shifts under climate change in two subspecies of Black-tailed Godwits in Asia

    Bing Run Zhu, Mo Verhoeven, Nicolas Velasco, Lisa Sanchez-Aguilar, Zhengwang Zhang, Theunis Piersma

    Habitat loss and shifts associated with climate change threaten global biodiversity, with impacts likely to be most pronounced at high latitudes. With the disappearance of the tundra breeding habitats, migratory shorebirds that breed at these high latitudes are likely to be even more vulnerable to climate change than those in temperate regions. We examined this idea using new distributional information on two subspecies of Black-tailed Godwits Limosa limosa in Asia: the northerly, bog-breeding L. l. bohaii and the more southerly, steppe-breeding L. l. melanuroides. Based on breeding locations of tagged and molecularly assayed birds, we modelled the current breeding distributions of the two subspecies with species distribution models, tested those models for robustness and then used them to predict climatically suitable breeding ranges in 2070 according to bioclimatic variables and different climate change scenarios. Our models were robust and showed that climate change is expected to push bohaii into the northern rim of the Eurasian continent. Melanuroides is also expected to shift northward, stopping in the Yablonovyy and Stanovoy Ranges, and breeding elevation is expected to increase. Climatically suitable breeding habitat ranges would shrink to 16% and 11% of the currently estimated ranges of bohaii and melanuroides, respectively. Overall, this study provides the first predictions for the future distributions of two little-known Black-tailed Godwit subspecies and highlights the importance of factoring in shifts in bird distribution when designing climate-proof conservation strategies.

    https://doi.org/10.1111/gcb.16308
  • Ecological Solutions and Evidence
    2022

    Do ditch‐side electric fences improve the breeding productivity of ground‐nesting waders?

    Mo Verhoeven, A.H. Jelle Loonstra, Thomas Pringle, Wiebe Kaspersma, Mark Whiffin, Alice D. McBride, Pieter Sjoerdsma, Celine Roodhart, Malcolm D. Burgess, Theunis Piersma, Jennifer Smart
    Insufficient reproduction as a consequence of predation on eggs and chicks is a major determinant of population decline in ground-nesting birds, including waders. For many populations, there is an urgent need to maintain breeding populations at key sites, and conservation practitioners need to find viable management solutions to reduce predation. One tool available to the practitioner is fences that exclude key predators from areas containing breeding birds. Temporary electric fencing is an increasingly popular predator exclusion intervention, but such fences have costs associated with purchase and the time needed to erect and maintain them. Their effectiveness and optimal application are also frequently questioned. We evaluate the use of temporary ditch-side four-strand electric fences in lowland grasslands in two countries, The Netherlands and England, in areas containing high densities of breeding waders. In both countries and in all years, godwit and lapwing nest survival was significantly higher within areas enclosed by ditch-side electric fences. Brood survival, assessed for godwits in The Netherlands, was also higher within fenced areas in all years. This demonstrates that using temporary electric fences to enclose ground-nesting birds can be an effective tool for improving breeding productivity. In our study, closely managed electric fences were effective at excluding red foxes Vulpes vulpes, but not avian and other mammalian predators. The positive effect that electric fencing had on nest and brood survival therefore likely results from a reduction in the total number of visits by mammalian predators, and especially visits by foxes. Although it requires a substantial time investment throughout the period of use, our temporary electric fence design provides flexibility compared to other fence designs when it comes to enclosing different areas within a season and between years, as the targets for protection change or as land and flood management dictate. This conservation intervention can help buy the time required to develop and implement longer term solutions for application at larger scales.
    https://doi.org/10.1002/2688-8319.12143
  • Methods in Ecology and Evolution
    2022

    Misidentification errors in reencounters result in biased estimates of survival probability from CJS models

    Eldar Rakhimberdiev, Julia Karagicheva, Anatoly Saveliev, A.H. Jelle Loonstra, Mo Verhoeven, Jos C.E.W. Hooijmeijer, Michael Schaub, Theunis Piersma

    Misidentification of marked individuals is unavoidable in most studies of wild animal populations. Models commonly used for the estimation of survival from such capture–recapture data ignore misidentification errors potentially resulting in biased parameter estimates. With a simulation study, we show that ignoring misidentification in Cormack–Jolly–Seber (CJS) models results in systematic positive biases in the estimates of survival and in spurious declines of survival over time. We developed an extended robust design capture mark–resight (RDM) model that includes correct identification parameters to get unbiased survival estimates when resighting histories are prone to misidentification. The model assumes that resightings occur repeatedly within a season, which in practice is often the case when resightings of colour-marked individuals are collected. We implemented the RDM model in a state-space formulation and also an approximate, but computationally faster, model (RDMa) in JAGS and evaluated their performances using simulated and empirical capture–resight data on black-tailed godwits Limosa limosa. The CJS models applied to simulated data under an imperfect identification scenario data produced strongly positively biased estimates of survival. For a range of degrees of correct identification probabilities, the RDM model provided unbiased and accurate estimates of survival, reencounter and correct-identification probabilities. The RDMa model performed well for large datasets (>25 individuals), with high resighting (>0.3) and high correct identification (>0.7) probabilities. For the empirical data, the CJS model estimated average juvenile survival at 0.997% and adult survival at 0.939% and also detected a strong decline in adult survival over time at a rate of −0.14 ± 0.029. In contrast, the RDMa model estimated a probability of correct identification of 0.94, annual juvenile survival at 0.234%, adult at 0.834% and less strong decline over time (−0.046 ± 0.016). We conclude that estimates of survival probabilities obtained from data that include misidentification errors and analysed with standard CJS model are unlikely to be correct. The bias in survival increases with the magnitude of misidentification errors, which is inevitable as datasets become longer. Since misidentification due to tag misreads is common in empirical data, we recommend the use of the here presented RDM model to provide unbiased parameter estimates.

    https://doi.org/10.1111/2041-210X.13825
  • Ecological Solutions and Evidence
    2022

    Earthworm abundance and availability does not influence the reproductive decisions of black-tailed godwits in an agricultural grassland

    Mo Verhoeven, Alice D. McBride, Jos C.E.W. Hooijmeijer, Theunis Piersma, Nathan R Senner

    Maintaining the biodiversity of agricultural ecosystems has become a global imperative. Across Europe, species that occupy agricultural grasslands, such as black-tailed godwits (Limosa limosa limosa), have undergone steep population declines. In this context, there is a significant need to both determine the root causes of these declines and identify actions that will promote biodiversity while supporting the livelihoods of farmers. Food availability, and specifically earthworm abundance (Lumbricidae), during the pre-breeding period has often been suggested as a potential driver of godwit population declines. Previous studies have recommended increasing the application of nitrogen to agricultural grasslands to enhance earthworm populations and aid agricultural production. Here we test whether food availability during the pre-breeding period affects when and where godwits breed. Using large-scale surveys of food availability, a long-term mark-recapture study, focal observations of foraging female godwits, and tracking devices that monitored godwit movements, we found little evidence of a relationship between earthworm abundance and the timing of godwit reproductive efforts or the density of breeding godwits. Furthermore, we found that the soils of intensively managed agricultural grasslands may frequently be too dry for godwits to forage for those earthworms that are present. The increased application of nitrogen to agricultural grasslands will therefore likely have no positive effect on godwit populations. Instead, management efforts should focus on increasing the botanical diversity of agricultural grasslands, facilitating conditions that prevent hardening soils, and reducing the populations of generalist predators.

    https://doi.org/10.1002/2688-8319.12125
  • Journal of Ornithology
    2022

    Cross-continental differences in Black-tailed Godwit breeding densities are best explained by arthropod abundance in the chick-hatching period

    Miguel Silva-Monteiro, Hannes Pehlak, Sami Timonen, Jorma Pessa, Esko Pasanen, Mo Verhoeven, A.H. Jelle Loonstra, Theunis Piersma, Frederic Robin, Michał Korniluk, Melissa Onwezen, Morten F. Bongers, Jaap Hamelink, Frederik Lembreght, Audrey Dunn, David Kleijn
    The endangered continental Black-tailed Godwit (Limosa limosa limosa) is a migratory ground-nesting wader breeding in a wide variety of open, wet habitats across Europe. Conservation research has concentrated on the causes of population decline, but we know surprisingly little about whether any resources limit local breeding populations and if so, whether these are resources for the adults or the chicks. We collected data from 63 key breeding sites in five countries across Europe to test whether, after correcting for differences in surveyed areas, the size of Godwit breeding populations was related to environmental variables (vegetation biomass, soil moisture) or food resources for adult birds (soil invertebrates) or chicks (vegetation dwelling arthropods) measured during different times of the reproductive cycle. We found the number of Godwit territories to be positively related to arthropod abundance during the chick-hatching period. We found additional, weaker support for a positive relation between Godwit territory numbers and the abundance of soil-dwelling invertebrates (mostly earthworms) at clutch laying, but not at chick-hatching. These relationships were observed across countries, while we found little support for relationships within countries, possibly due to the smaller range in conditions that exist within countries. Both vegetation growth and soil moisture weren’t related to Godwit territory numbers. Our results suggest that food abundance for chicks, and to a lesser extent adult birds, are key factors determining the size of local Godwit breeding populations. Conservation management aiming to enhance local Godwit populations should therefore consider the impacts of management strategies on the arthropod prey of chicks.
    https://doi.org/10.1007/s10336-022-02041-9
  • Wader Study
    04-2021

    Diagnosing the recent population decline of black-tailed godwits in the United Kingdom

    Mo Verhoeven, Jennifer Smart, Charlie Kitchin, Sabine Schmitt, Mark Whiffin, Malcolm D. Burgess, Norman Ratcliffe

    During the last 50 years, the breeding population of Continental Black-tailed Godwits Limosa limosa limosa in the United Kingdom has been relatively small (below 60 pairs) and largely concentrated in two locations in eastern England. There were severe declines at the Ouse Washes during the 1990s due to increased spring flooding. In the following years, there were increases at the nearby Nene Washes. However, since 2006, the population at the Nene Washes has been declining – from 48 pairs in 2006 to 37 pairs in 2014. With ~85% of the UK population relying on the Nene Washes, it is important to diagnose the cause of this decline. We do this by comparing adult, nest and chick survival estimates across two time periods when research projects were active: the ‘early’ period (1999–2003) when the population was rapidly increasing, and the ‘contemporary’ period (2015–2019), during the population decline. We found no clear difference in annual apparent adult survival rates between the two periods. However, both nest and chick survival were lower in the contemporary period (nest survival by 31–41% depending on lay date; chick survival by 59–72% depending on hatch date). We show that 61 of 63 Nene-hatched chicks known to have recruited did so back into the Nene Washes population. The recent decline is therefore not the result of changes in adult mortality or breeding dispersal, but insufficient breeding productivity leading to insufficient recruitment into the natal population. The decrease in nest survival in the contemporary period results from an increase in predation pressure, as only one nest was flooded and none were destroyed by agricultural activities. We discuss why predation pressure might have increased and whether this could also explain the observed change in chick survival. We go on to recommend research and management efforts that should be undertaken to stop further declines of this population in the short-and long-term.

    https://doi.org/10.18194/ws.00216
  • Journal of Ornithology
    01-2021

    Migration route, stopping sites, and non-breeding destinations of adult Black-tailed Godwits breeding in southwest Fryslân, The Netherlands

    Mo Verhoeven, A.H. Jelle Loonstra, Alice D. McBride, Christiaan Both, Nathan R Senner, Theunis Piersma

    In this paper, we extend our understanding of the migration of Black-tailed Godwits (Limosa limosa limosa) by describing: (1) the orientation and geographic locations of individual migratory routes and (2) the spatial distribution of godwits across seasons and years. We accomplish this using satellite-tracking data from 36 adult godwits breeding in the 200-ha Haanmeer polder in The Netherlands, from 2015 to 2018. During both southward and northward migration, godwits used a narrow migratory corridor along which most individuals made stops within a network of sites, especially the Bay of Biscay, France and Doñana, Spain. Most sites were used consistently by the same individuals across years. However, sites in Morocco were used during northward migration by 75% of individuals, but not revisited by the same individual across years. After southward migration, a small proportion (15%) of godwits spent the entire non-breeding period north of the Sahara, but most (85%) crossed the Sahara and spent at least part of the non-breeding season among seven coastal sites in West Africa and one site in the Inner Niger Delta. Although site-use patterns varied among individuals, individuals showed high site fidelity and were consistent in the number of sites they used from year to year. The considerable differences in the spatial distribution of individuals that breed within a kilometre of one another raise questions about the causes and consequences of individual migratory differences. We discuss that full annual cycle tracking of juveniles from birth to adulthood is needed to understand the source of these individual differences. Our results on the spatial distribution of godwits throughout their annual cycle lay an important foundation of information that can be used to help conserve this declining species.

    https://doi.org/10.1007/s10336-020-01807-3
  • Emu
    2021

    Identification of breeding grounds and annual routines of the newly discovered bohaii subspecies of Black-tailed Godwits

    Bing Run Zhu, Mo Verhoeven, A.H. Jelle Loonstra, Lisa Sanchez-Aguilar, Chris J. Hassell, Katherine K.S. Leung, Weipan Lei, Zhengwang Zhang, Theunis Piersma

    The Bohai Black-tailed Godwit (Limosa limosa bohaii) is a newly discovered subspecies in the East Asian-Australasian Flyway. Based on satellite tracking of 21 individuals that were tagged in northern Bohai Bay, China, from 2016 to 2018, we here describe the annual cycle of this subspecies. All the birds had Thailand as their southernmost ‘winter’ destination. The spring departure was in late March during northward migration, Bohai Bay was the first stopping site where they spent on average 39 days (± SD = 6 d), followed by Inner Mongolia and Jilin province (stopping for 8 d ± 1 d). The arrival of the breeding grounds in the Russian Far East was centred in late May. Two breeding sites were detected, with average locations 1100 km apart; the eastern site was beyond the known Asian breeding distribution of the Black-tailed Godwit. Southward migration started in late June, with the godwits tending to make longer stops at the same two main stopping sites used in the spring, i.e. Inner Mongolia and Jilin province (32 ± 5 d) and Bohai Bay (44 ± 8 d), with some individuals making a third stop in the middle-lower reaches of the Yangtze River in southern China (12 ± 4 d). By the end of September, most tracked individuals had arrived in Thailand. Compared with the previously known subspecies, bohaii godwits have strikingly different schedules of migration and moult, this study thus adding to the knowledge about intraspecific diversity of black-tailed godwits in the East Asian-Australian Flyway.

    https://doi.org/10.1080/01584197.2021.1963287
  • Ecology
    01-09-2020

    Full lifetime perspectives on the costs and benefits of lay-date variation in tree swallows

    David W. Winkler, Kelly K. Hallinger, Teresa M. Pegan, Conor C. Taff, Mo Verhoeven, David Chang van Oordt, Maria Stager, Jennifer J. Uehling, Maren N Vitousek, Michael J. Andersen, Daniel R. Ardia, Amos Belmaker, Valentina Ferretti, Anna M. Forsman, Jennifer R. Gaul, Paulo E. Llambias, Sophia C. Orzechowski, Jeremy Ryan Shipley, Maya Wilson, Hyun Seok Yoon

    Animals must balance various costs and benefits when deciding when to breed. The costs and benefits of breeding at different times have received much attention, but most studies have been limited to investigating short-term season-to-season fitness effects. However, breeding early, versus late, in a season may influence lifetime fitness over many years, trading off in complex ways across the breeder’s lifespan. In this study, we examined the complete life histories of 867 female tree swallows (Tachycineta bicolor) breeding in Ithaca, New York, between 2002 and 2016. Earlier breeders outperformed later breeders in short-term measures of reproductive output and offspring quality. Though there were weak indications that females paid long-term future survival costs for breeding early, lifetime fledgling output was markedly higher overall in early-breeding birds. Importantly, older females breeding later in the season did not experience compensating life history advantages that suggested an alternative equal-fitness breeding strategy. Rather, most or all of the swallows appear to be breeding as early as they can, and differences in lay dates appear to be determined primarily by differences in individual quality or condition. Lay date had a significant repeatability across breeding attempts by the same female, and the first lay date of females fledged in our population was strongly influenced by the first lay date of their mothers, indicating the potential for ongoing selection on lay date. By examining performance over the entire lifespan of a large number of individuals, we were able to clarify the relationship between timing of breeding and fitness and gain new insight into the sources of variability in this important life history trait.

    https://doi.org/10.1002/ecy.3109
  • Journal of Avian Biology
    01-05-2020

    Rethinking classic starling displacement experiments

    Theunis Piersma, A.H. Jelle Loonstra, Mo Verhoeven, Thomas Oudman

    In an attempt to encourage the discourse on sources of individual variation in seasonal migration patterns and the microevolution of bird migration, we here critically examine the published interpretations of a now classic displacement study with starlings Sturnus vulgaris. Based on the ring recoveries after experimental displacement towards the south and southeast of Dutch capture sites of over 18 000 hatch-year and older starlings, in a series of analyses published in Ardea from 1958 to 1983, A. C. Perdeck established that displaced starlings showed appropriately changed orientations only when they were experienced. During both southward and northward migration, released adults navigated to an apparently previously learned goal (i.e. the wintering or the breeding area) by showing appropriately changed orientations. Juveniles showed appropriate directions when returning to the breeding grounds. In contrast, during their first southward migration displaced juveniles carried on in the direction (and possibly the distance) expected for their release at the Dutch capture site. From the mid-1970s this work has become cited as evidence for starlings demonstrating ‘innate’ migratory directions. If the definition of innateness is ‘not learned by the individual itself’, then there is a range of non-innate influences on development that are not ruled out by Perdeck's experimental outcomes. For example, young starlings might have carried on in the direction that they learned to migrate before being caught, e.g. by observing the migratory directions of experienced conspecifics. We argue that, despite over 60 citations to Perdeck as demonstrating innate migratory directions, the jury is out.

    https://doi.org/10.1111/jav.02337
  • Journal of Avian Biology
    01-04-2020

    Geolocators lead to better measures of timing and renesting in black-tailed godwits and reveal the bias of traditional observational methods

    Mo Verhoeven, A.H. Jelle Loonstra, Alice D. McBride, Pablo Macias, Wiebe Kaspersma, Jos C.E.W. Hooijmeijer, Egbert van der Velde, Christiaan Both, Nathan R Senner, Theunis Piersma

    Long-term population studies can identify changes in population dynamics over time. However, to realize meaningful conclusions, these studies rely on accurate measurements of individual traits and population characteristics. Here, we evaluate the accuracy of the observational methods used to measure reproductive traits in individually marked black-tailed godwits (Limosa limosa limosa). By comparing estimates from traditional methods with data obtained from light-level geolocators, we provide an accurate estimate of the likelihood of renesting in godwits and the repeatability of the lay dates of first clutches. From 2012 to 2018, we used periods of shading recorded on the light-level geolocators carried by 68 individual godwits to document their nesting behaviour. We then compared these estimates to those simultaneously obtained by our long-term observational study. We found that among recaptured geolocator-carrying godwits, all birds renested after a failed first clutch, regardless of the date of nest loss or the number of days already spent incubating. We also found that 43% of these godwits laid a second replacement clutch after a failed first replacement, and that 21% of these godwits renested after a hatched first clutch. However, the observational study correctly identified only 3% of the replacement clutches produced by geolocator-carrying individuals and designated as first clutches a number of nests that were actually replacement clutches. Additionally, on the basis of the observational study, the repeatability of lay date was 0.24 (95% CI 0.17–0.31), whereas it was 0.54 (95% CI 0.28–0.75) using geolocator-carrying individuals. We use examples from our own and other godwit studies to illustrate how the biases in our observational study discovered here may have affected the outcome of demographic estimates, individual-level comparisons, and the design, implementation and evaluation of conservation practices. These examples emphasize the importance of improving and validating field methodologies and show how the addition of new tools can be transformational.

    https://doi.org/10.1111/jav.02259
  • Ardea
    01-12-2019

    Variation in Egg Size of Black-Tailed Godwits

    Mo Verhoeven, A.H. Jelle Loonstra, Alice D. McBride, J.M. Tinbergen, Rosemarie Kentie, Jos C.E.W. Hooijmeijer, Christiaan Both, Nathan R Senner, Theunis Piersma

    As is the case for most avian species, there is considerable variation in the egg size of Continental Black-tailed Godwits Limosa l. limosa breeding in The Netherlands. It is interesting that egg size has costs and benefits yet varies considerably at the population level. To better understand this variation in egg size, we tested its relationship to a suite of individual and environmental factors. We found that egg size can decrease up to 2.8% throughout a breeding season and that egg size increases with clutch size by 1.4% with each additional egg in the clutch. Female body mass and body size explained 5% of the total variation in egg size observed across the population. Furthermore, females wintering south of the Sahara laid 3% smaller eggs than those wintering north of the Sahara. We also found that egg size increases with age, which may indicate age-related differences in the endogenous and/or exogenous conditions of females. The variation in egg size was, however, mostly the result of consistent differences among individuals across years (repeatability = 0.60). A comparison of daughters with mothers suggested that most of this individual repeatability reflects heritable variation (heritability = 0.64). The actual individual traits that underlie this heritable variation among individuals remain mostly undetermined. Smaller eggs did have a slightly lower chance of hatching, but we found no relationship between egg size and chick survival. Finally, nest and chick survival were strongly correlated with lay date. Thus, in Black-tailed Godwits, lay date may actually reflect a female's endogenous and/or exogenous condition at the moment of egg-laying. This finding may be general across birds, since food supplementation experiments usually result in advanced laying and larger clutch sizes rather than in larger eggs.

    https://doi.org/10.5253/arde.v107i3.a7
  • Ardea
    01-12-2019

    Individual Black-Tailed Godwits Do Not Stick to Single Routes

    A.H. Jelle Loonstra, Mo Verhoeven, Adam Zbyryt, Ester Schaaf, Christiaan Both, Theunis Piersma

    The miniaturization of tracking devices is now rapidly increasing our knowledge on the spatiotemporal organization of seasonal migration. So far, most studies aimed at understanding within- and between-individual variation in migratory routines focus on single populations. This has also been the case for continental Black-tailed Godwits Limosa l. limosa (hereafter Godwits), with most work carried out on individuals from the Dutch breeding population, migrating in relatively large numbers in the westernmost part of the range. Here we report the migratory timing and routes of four adult individuals of the same subspecies from the low-density population in eastern Poland and compare this with previously published data on Godwits breeding in The Netherlands. During northward migration, the birds from Poland departed and arrived later from their wintering and breeding grounds. However, on southward migration the Polish breeding Godwits departed earlier, but arrived one month later than the Dutch birds on their wintering grounds in sub-Saharan Africa. Despite the small sample size of tracked birds from Poland, we find a significantly higher between-individual variation in timing during southward migration in Polish Godwits as compared to the Dutch Godwits. Furthermore, not only did migratory routes differ, but the few Polish Godwits tracked showed a higher level of between- and within-individual variation in route choice during both southward and northward migration. To explain this remarkable discrepancy, we propose that the properties of transmission of social information may be different between Godwits from a high-density population (i.e. the one in The Netherlands) and a low-density population (in Poland) and that this leads to different levels of canalization. To examine this hypothesis, future studies should not only follow individuals from an early age onwards, but also quantify and experimentally manipulate their social environments during migration.

    https://doi.org/10.5253/arde.v107i3.a11
  • Behavioral Ecology
    13-06-2019

    Natal habitat and sex-specific survival rates result in a male-biased adult sex ratio

    A.H. Jelle Loonstra, Mo Verhoeven, Nathan R Senner, Jos C.E.W. Hooijmeijer, Theunis Piersma, Rosemarie Kentie

    The adult sex ratio (ASR) is a crucial component of the ecological and evolutionary forces shaping the dynamics of a population. Although in many declining populations ASRs have been reported to be skewed, empirical studies exploring the demographic factors shaping ASRs are still rare. In this study of the socially monogamous and sexually dimorphic Black-tailed Godwit (Limosa limosa limosa), we aim to evaluate the sex ratio of chicks at hatch and the subsequent sex-specific survival differences occurring over 3 subsequent life stages. We found that, at hatch, the sex ratio did not deviate from parity. However, the survival of pre-fledged females was 15-30% lower than that of males and the sex bias in survival was higher in low-quality habitat. Additionally, survival of adult females was almost 5% lower than that of adult males. Because survival rates of males and females did not differ during other life-history stages, the ASR in the population was biased toward males. Because females are larger than males, food limitations during development or sex-specific differences in the duration of development may explain the lower survival of female chicks. Differences among adults are less obvious and suggest previously unknown sex-related selection pressures. Irrespective of the underlying causes, by reducing the available number of females in this socially monogamous species, a male-biased ASR is likely to contribute to the ongoing decline of the Dutch godwit population.

    https://doi.org/10.1093/beheco/arz021
  • Frontiers in Ecology and Evolution
    2019

    Variation from an unknown source

    Mo Verhoeven, A.H. Jelle Loonstra, Nathan R Senner, Alice D. McBride, Christiaan Both, Theunis Piersma

    Variation in migratory behavior is the result of different individual strategies and fluctuations in individual performances. A first step toward understanding these differences in migratory behavior among individuals is, therefore, to assess the relative contributions of inter- and intra-individual differences to this variation. We did this using light-level geolocators deployed on the breeding grounds to follow continental black-tailed godwits (Limosa limosa limosa) throughout their south- and northward migrations over multiple years. Based on repeated tracks from 36 individuals, we found two general patterns in godwit migratory behavior: First, migratory timing in black-tailed godwits varies mostly because individual godwits migrate at different times of the year. Second, individuals also exhibit considerable variation in timing within their respective migratory windows. Although the absolute amount of inter-individual variation in timing decreased over the course of northward migration, individual godwits still arrived at their breeding grounds across a span of more than 5 weeks. These differences in migratory timing among individuals are larger than those currently observed in other migratory bird species and suggest that the selective forces that limit the variation in migratory timing in other species are relaxed or absent in godwits. Furthermore, we could not attribute these individual differences to the sex or wintering location of an individual. We suggest that different developmental trajectories enabled by developmental plasticity likely result in these generally consistent, life-long annual routines. To investigate this possibility and to gain an understanding of the different selection pressures that could be acting during migration and throughout a godwit's life, future studies should track juvenile godwits and other migratory birds from birth to adulthood while also manipulating their spatiotemporal environment during development.

    https://doi.org/10.3389/fevo.2019.00031
  • Frontiers in Ecology and Evolution
    2019

    High migratory survival and highly variable migratory behavior in black-tailed godwits

    Nathan R Senner, Mo Verhoeven, José M. Abad-Gómez, José A Alves, Jos C.E.W. Hooijmeijer, Ruth A. Howison, Rosemarie Kentie, A.H. Jelle Loonstra, José A. Masero, Afonso Rocha, Maria Stager, Theunis Piersma

    Few studies have been able to directly measure the seasonal survival rates of migratory species or determine how variable the timing of migration is within individuals and across populations over multiple years. As such, it remains unclear how likely migration is to affect the population dynamics of migratory species and how capable migrants may be of responding to changing environmental conditions within their lifetimes. To address these questions, we used three types of tracking devices to track individual black-tailed godwits from the nominate subspecies (Limosa limosa limosa) throughout their annual cycles for up to 5 consecutive years. We found that godwits exhibit considerable inter- and intra-individual variation in their migratory behavior across years. We also found that godwits had generally high survival rates during migration, although survival was reduced during northward flights across the Sahara Desert. These patterns differ from those observed in most other migratory species, suggesting that migration may only be truly dangerous when crossing geographic barriers that lack emergency stopover sites and that the levels of phenotypic flexibility exhibited by some populations may enable them to rapidly respond to changing environmental conditions.

    https://doi.org/10.3389/fevo.2019.00096
  • Global Change Biology
    11-2018

    Warming springs and habitat alteration interact to impact timing of breeding and population dynamics in a migratory bird

    Rosemarie Kentie, Tim Coulson, Jos C.E.W. Hooijmeijer, Ruth A. Howison, A.H. Jelle Loonstra, Mo Verhoeven, Christiaan Both, Theunis Piersma

    In seasonal environments, increasing spring temperatures lead many taxa to advance the timing of reproduction. Species that do not may suffer lower fitness. We investigated why black-tailed godwits (Limosa limosa limosa), a ground-breeding agricultural grassland shorebird, have not advanced timing of reproduction during the last three decades in the face of climate change and human-induced habitat degradation. We used data from an 11-year field study to parameterize an Integral Projection Model to predict how spring temperature and habitat quality simultaneously influence the timing of reproduction and population dynamics. We found apparent selection for earlier laying, but not a correlation between the laying dates of parents and their offspring. Nevertheless, in warmer springs, laying dates of adults show a stronger positive correlation with laying date in previous springs than in cooler ones, and this leads us to predict a slight advance in the timing of reproduction if spring temperatures continue to increase. We also show that only in landscapes with low agricultural activity, the population can continue to act as a source. This study shows how climate change and declining habitat quality may enhance extinction risk.

    https://doi.org/10.1111/gcb.14406
  • Proceedings of the Royal Society B: Biological Sciences
    27-06-2018

    High-altitude shorebird migration in the absence of topographical barriers

    Nathan R Senner, Maria Stager, Mo Verhoeven, Zachary A. Cheviron, Theunis Piersma, Willem Bouten

    Nearly 20% of all bird species migrate between breeding and nonbreeding sites annually. Their migrations include storied feats of endurance and physiology, from non-stop trans-Pacific crossings to flights at the cruising altitudes of jetliners. Despite intense interest in these performances, there remains great uncertainty about which factors most directly influence bird behaviour during migratory flights. We used GPS trackers that measure an individual’s altitude and wingbeat frequency to track the migration of black-tailed godwits (Limosa limosa) and identify the abiotic factors influencing their in-flight migratory behaviour. We found that godwits flew at altitudes above 5000 m during 21% of all migratory flights, and reached maximum flight altitudes of nearly 6000 m. The partial pressure of oxygen at these altitudes is less than 50% of that at sea level, yet these extremely high flights occurred in the absence of topographical barriers. Instead, they were associated with high air temperatures at lower altitudes and increasing wind support at higher altitudes. Our results therefore suggest that wind, temperature and topography all play a role in determining migratory behaviour, but that their relative importance is context dependent. Extremely high-altitude flights may thus not be especially rare, but they may only occur in very specific environmental contexts.

    https://doi.org/10.1098/rspb.2018.0569
  • Bird Study
    02-01-2018

    Primary moult of continental Black-tailed Godwits Limosa limosa limosa in the Doñana wetlands, Spain

    Rocío Márquez-Ferrando, Magdalena Remisiewicz, José A. Masero, Rosemarie Kentie, Nathan R Senner, Mo Verhoeven, Jos C.E.W. Hooijmeijer, Sara Pardal, Mathieu Sarasa, Theunis Piersma, Jordi Figuerola

    Capsule: Most Continental Black-tailed Godwits Limosa limosa limosa using the Doñana wetlands during post-breeding migration appear to begin moult before they arrive and suspend moult before they migrate onwards to West Africa. Aims: We aim to describe the primary moult strategies and patterns in the Continental Black-tailed Godwits using the Doñana wetlands, a major passage and wintering area for waterbirds in southern Spain. Methods: Individual godwits were captured, marked and their primary moult was scored in Doñana during the non-breeding season (June–March) in 2011 and 2012. Data from resightings of colour-marked godwits and birds equipped with satellite transmitters were used to estimate stopover duration during post-breeding migration (June–September) to determine if godwits move to West Africa before completing their primary moult. Results: Average primary moult duration was estimated to be 84 days ± 9 se, during 29 June–21 September and did not differ between sexes. Only 2% of individuals were observed with suspended moult. We estimated stopover duration in Doñana to be 13 days ± 2 se before migrating to West Africa. Conclusions: Most godwits stage for about two weeks in the Doñana wetlands during southward migration, moult their primaries and appear to suspend moult before crossing the Sahara. Others may complete their primary moult in Doñana, or elsewhere in Europe and overwinter in Doñana where increasing numbers of godwits have been detected in recent years. A few individuals may finish the moult in Doñana and migrate to West Africa late in the post-breeding season.

    https://doi.org/10.1080/00063657.2018.1443055
  • Ibis
    01-2018

    Sex-specific growth in chicks of the sexually dimorphic Black-tailed Godwit

    A.H. Jelle Loonstra, Mo Verhoeven, Theunis Piersma

    Sexual size dimorphism (SSD) is common in birds and has been linked to various selective forces. Nevertheless, the question of how and when the sexes start to differentiate from each other is poorly studied. This is a critical knowledge gap, as sex differences in growth may cause different responses to similar ecological conditions. In this study, we describe the sex-specific growth – based on body mass and five morphometric measurements – of 56 captive Black-tailed Godwit Limosa limosa limosa chicks raised under ad libitum food conditions, and conclude that all six growth curves are sex-specific. Females are the larger sex in terms of body mass and skeletal body size. To test whether sex-specific growth leads to sex-specific susceptibility to environmental conditions, we compared the age-specific sizes of male and female chicks in the wild with those of Black-tailed Godwits reared in captivity. We then tested for a relationship between residual growth and relative hatching date, age, sex and habitat type in which the wild chicks were born. Early-hatched chicks were relatively bigger and in better condition than late-hatched chicks, but body condition and size were not affected by natal habitat type. Female chicks deviated more negatively from the sex-specific growth curves than male chicks for body mass and total-head length. This suggests that the growth of the larger females is more susceptible to limiting environmental conditions. On average, the deviations of wild chicks from the predicted growth curves were negative for all measurements, which suggests that conditions are limiting in the current agricultural landscape. We argue that in estimating growth curves for sexually dimorphic species, it is critical first to make accurate sex and age determinations.

    https://doi.org/10.1111/ibi.12541
  • Biology Letters
    2018

    Generational shift in spring staging site use by a long-distance migratory bird

    Mo Verhoeven, A.H. Jelle Loonstra, Jos C.E.W. Hooijmeijer, José A. Masero, Theunis Piersma, Nathan R Senner

    In response to environmental change, species have been observed altering their migratory behaviours. Few studies, however, have been able to determine whether these alterations resulted from inherited, plastic or flexible changes. Here, we present a unique observation of a rapid population-level shift in migratory routes—over 300 km from Spain to Portugal—by continental black-tailed godwits Limosa limosa limosa. This shift did not result from adult godwits changing staging sites, as adult site use was highly consistent. Rather, the shift resulted from young godwits predominantly using Portugal over Spain. We found no differences in reproductive success or survival among individuals using either staging site, indicating that the shift resulted from developmental plasticity rather than natural selection. Our results therefore suggest that new migratory routes can develop within a generation and that young individuals may be the agents of such rapid changes.

    https://doi.org/10.1098/rsbl.2017.0663
  • Ecology and Evolution
    04-2017

    Does wintering north or south of the Sahara correlate with timing and breeding performance in black-tailed godwits?

    Rosemarie Kentie, Rocío Márquez-Ferrando, Jordi Figuerola, Laura Gangoso, Jos C.E.W. Hooijmeijer, A.H. Jelle Loonstra, Frédéric Robin, Mathieu Sarasa, Nathan R Senner, Haije Valkema, Mo Verhoeven, Theunis Piersma

    Migrating long distances requires time and energy, and may interact with an individual's performance during breeding. These seasonal interactions in migratory animals are best described in populations with disjunct nonbreeding distributions. The black-tailed godwit (Limosa limosa limosa), which breeds in agricultural grasslands in Western Europe, has such a disjunct nonbreeding distribution: The majority spend the nonbreeding season in West Africa, while a growing number winters north of the Sahara on the Iberian Peninsula. To test whether crossing the Sahara has an effect on breeding season phenology and reproductive parameters, we examined differences in the timing of arrival, breeding habitat quality, lay date, egg volume, and daily nest survival among godwits (154 females and 157 males), individually marked in a breeding area in the Netherlands for which wintering destination was known on the basis of resightings. We also examined whether individual repeatability in arrival date differed between birds wintering north or south of the Sahara. Contrary to expectation, godwits wintering south of the Sahara arrived two days earlier and initiated their clutch six days earlier than godwits wintering north of the Sahara. Arrival date was equally repeatable for both groups, and egg volume larger in birds wintering north of the Sahara. Despite these differences, we found no association between wintering location and the quality of breeding habitat or nest survival. This suggests that the crossing of an important ecological barrier and doubling of the migration distance, twice a year, do not have clear negative reproductive consequences for some long-distance migrants.

    https://doi.org/10.1002/ece3.2879
  • Ardea
    12-2016

    Estimating the size of the Dutch breeding population of continental black-tailed godwits from 2007-2015 using resighting data from spring staging sites

    Rosemarie Kentie, Nathan R Senner, Jos C.E.W. Hooijmeijer, Rocío Márquez-Ferrando, Jordi Figuerola, José A. Masero, Mo Verhoeven, Theunis Piersma

    Over the past 50 years, the population of Continental Black-tailed Godwits Limosa limosa limosa breeding of the East Atlantic Flyway has been in steep decline. This decline has previously been documented in trend analyses and six Netherlands-wide count-based population estimates, the last of which was completed in 1999. We provide an updated population size estimate and describe inter-annual fluctuations in the population between 2007 and 2015. To generate these estimates, we integrated a mark-recapture survival analysis with estimates of the densities of colour-marked individuals at migratory staging sites with known proportions of Continental and Icelandic L. l. islandica Black-tailed Godwits within a Bayesian framework. The use of these analytical techniques means that, in contrast with earlier efforts, our estimates are accompanied with confidence intervals, allowing us to estimate the population size with known precision. Using additional information on the breeding destination of 43 godwits equipped with satellite transmitters at Iberian staging areas, we found that 87% (75-95% 95% CI) of the nominate subspecies in the East Atlantic Flyway breed in The Netherlands. We estimated that the number of breeding pairs in The Netherlands has declined from 47,000 (38,000-56,000) pairs in 2007 to 33,000 (26,000-41,000) in 2015. Despite a temporary increase in 2010 and 2011, the population declined by an average of 3.7% per year over the entire period from 2007-2015, and by 6.3% from 2011-2015. We conclude that investing in an intensive demographic programme at a regional scale, when combined with targeted resightings of marked individuals elsewhere, can yield population estimates at the flyway scale.

    https://doi.org/10.5253/arde.v104i3.a7
  • Journal of Avian Biology
    01-07-2016

    Comparing inferences of solar geolocation data against high-precision GPS data

    Eldar Rakhimberdiev, Nathan R Senner, Mo Verhoeven, David W. Winkler, Willem Bouten, Theunis Piersma

    Annual routines of migratory birds inferred from archival solar geolocation devices have never before been confirmed using GPS technologies. A female black-tailed godwit Limosa limosa limosa captured on the breeding grounds in the Netherlands in 2013 and recaptured in 2014 was outfitted with both an Intigeo geolocator and an UvA-BiTS GPS-tracker. The GPS positions show that, after its breeding season in 2013, the godwit flew 2035 km nonstop from the Netherlands to southern Spain. It then spent the entire nonbreeding season in the southern part of the Iberian Peninsula before returning to the Netherlands the following spring, stopping for 7 days in the delta of the Ebro River in Spain, and again for a day in central Belgium. To compare the geolocation and GPS data, we analysed the geolocation data with two open-source software packages: one using a threshold method (GeoLight) and the other a template-fit approach (FLightR). Estimates using GeoLight, on average, deviated from the individual's true position by 495.5 ± 1031.2 km (great circle distance with equinoxes excluded), while FLightR estimates deviated by 43.3 ± 51.5 km (great circle distance with equinoxes included). Arrival and departure schedules estimated by FLightR were within 12 h of those determined by the GPS tracker, whereas GeoLight's estimates were less precise. For the analysed track, FLightR represents an improvement over GeoLight; if true for other species and conditions, FLightR will hopefully help establish more precise and accurate uses of geolocation data in tracking studies. To aid future improvements in the analysis of solar geolocation data, we also provide the GPS and geolocation data files together with our R scripts as Supplementary material Appendix 1–6.

    https://doi.org/10.1111/jav.00891
  • Emu
    2016

    Fuelling and moult in Red Knots before northward departure

    Mo Verhoeven, Joop Van Eerbeek, Chris J. Hassell, Theunis Piersma

    The departure of migratory birds from their non-breeding grounds is thought to be driven by the phenology of their breeding destination. In north-west Australia, two plumage morphs of Red Knot (Calidris canutus) prepare for a 5500-km journey to Yellow Sea staging areas. These morphs are recognised as the subspecies C. c. piersmai and C. C. Rogersi, which breed at different latitudes and have different seasonalities. From February to May 2011, we observed the migratory preparation of individually marked birds of known age, sex and type. This enabled a comparison of fuelling rates and pre-alternate moult among these classes. First-year birds did not prepare for migration. Second-year birds accumulated smaller fuel stores and reached lower plumage scores than adults. Adults of both types reached their highest abdominal profile scores by the end of April when they were last observed in Roebuck Bay. This lack of difference between types in the timing of fuelling and departure is surprising. Based on the differences in staging and breeding phenology, C. C. Rogersi is expected to leave north-west Australia 2-4 weeks before C. c. piersmai. Assuming that types and subspecies are equivalent, our findings in combination with other research on Red Knots in the East Asian-Australasian Flyway suggest that it takes more than breeding origin alone to explain annual cycles in migratory birds. Concurrent migratory schedules imply that, during northward staging in the Yellow Sea, there is strong variation in fuelling rates between and within subspecies depending on non-breeding origin. The ongoing loss of staging habitat may therefore have differential effects on Red Knots in the East Asian-Australasian Flyway.

    https://doi.org/10.1071/MU15035
  • Journal of Animal Ecology
    01-09-2015

    When Siberia came to the Netherlands

    Nathan R Senner, Mo Verhoeven, José M. Abad-Gómez, Jorge S. Gutiérrez, Jos C.E.W. Hooijmeijer, Rosemarie Kentie, José A. Masero, T Lee Tibbitts, Theunis Piersma

    Extreme weather events have the potential to alter both short- and long-term population dynamics as well as community- and ecosystem-level function. Such events are rare and stochastic, making it difficult to fully document how organisms respond to them and predict the repercussions of similar events in the future. To improve our understanding of the mechanisms by which short-term events can incur long-term consequences, we documented the behavioural responses and fitness consequences for a long-distance migratory bird, the continental black-tailed godwit Limosa limosa limosa, resulting from a spring snowstorm and three-week period of record low temperatures. The event caused measurable responses at three spatial scales - continental, regional and local - including migratory delays (+19 days), reverse migrations (>90 km), elevated metabolic costs (+8·8% maintenance metabolic rate) and increased foraging rates (+37%). There were few long-term fitness consequences, however, and subsequent breeding seasons instead witnessed high levels of reproductive success and little evidence of carry-over effects. This suggests that populations with continued access to food, behavioural flexibility and time to dissipate the costs of the event can likely withstand the consequences of an extreme weather event. For populations constrained in one of these respects, though, extreme events may entail extreme ecological consequences.

    https://doi.org/10.1111/1365-2656.12381
  • Wader Study
    06-2015

    Just when you thought you knew it all

    Nathan R Senner, Mo Verhoeven, Jos C.E.W. Hooijmeijer, Theunis Piersma

    Global climate change is rapidly altering the phenology and behaviour of species, leading to the occurrence of new and extreme trait values, especially among long-distance migratory birds. While infrequently published, the documentation and regular revision of the known spectrum of these trait values can be valuable for identifying the selective pressures acting on a population and influencing best management and conservation practices. Here we argue that the previously documented spectrum of reproductive behaviours in the rapidly declining Continental Black-tailed Godwit Limosa limosa limosa is in need of revision. Our data show that new extreme values for a number of reproductive traits occurred during the 2014 breeding season and that by almost every metric, 2014 had the longest laying period on record for the population. These findings suggest that godwit reproductive biology may be more flexible than previously thought and that this flexibility should be reflected by changes in European meadowbird policies.

    https://doi.org/10.18194/ws.00006

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