Christa Mateman

Ing. Christa Mateman

Technician

Bezoekadres

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands

Over

As a technician for the Animal Ecology department I am involved in the molecular analysis of samples. We use a relational database for collection management which makes it possible to compare phenotype with genotypes.

Biografie

Ing. Christa Mateman (1970) graduated as biochemical technician in 1993 at the "Hogeschool Enschede". In her final year she worked as a student at the NIZO (Netherlands Institute for Dairy Research) developing markers for detection and identification of lactic acid bacteria. She started working for the NIOO in 1993, initially for the Department of Plant Population Biology and subsequently for the Department of Animal Ecology. Her work involves developing techniques for sexing birds, screening for extra pair copulation's (microsatellites), studying genetic variation (next generation sequencing, SNP-detection) and gene expression (qPCR). She is also involved in the management of the samples collected within the department.

Onderzoeksgroepen

CV

Publicaties

Peer-reviewed publicaties

  • 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
  • Molecular Ecology Resources
    2022

    epiGBS2

    F. Gawehns, Maarten Postuma, Morgane Van Antro, Adam Nunn, Bernice Sepers, Samar Fatma, Thomas Van Gurp, Niels C. A. M. Wagemaker, A.C. Mateman, Slavica Milanovic-Ivanovic, Ivo Groβe, Kees van Oers, Philippine Vergeer, Koen Verhoeven

    Several reduced-representation bisulfite sequencing methods have been developed in recent years to determine cytosine methylation de novo in nonmodel species. Here, we present epiGBS2, a laboratory protocol based on epiGBS with a revised and user-friendly bioinformatics pipeline for a wide range of species with or without a reference genome. epiGBS2 is cost- and time-efficient and the computational workflow is designed in a user-friendly and reproducible manner. The library protocol allows a flexible choice of restriction enzymes and a double digest. The bioinformatics pipeline was integrated in the Snakemake workflow management system, which makes the pipeline easy to execute and modular, and parameter settings for important computational steps flexible. We implemented bismark for alignment and methylation analysis and we preprocessed alignment files by double masking to enable single nucleotide polymorphism calling with Freebayes (epiFreebayes). The performance of several critical steps in epiGBS2 was evaluated against baseline data sets from Arabidopsis thaliana and great tit (Parus major), which confirmed its overall good performance. We provide a detailed description of the laboratory protocol and an extensive manual of the bioinformatics pipeline, which is publicly accessible on github (https://github.com/nioo-knaw/epiGBS2) and zenodo (https://doi.org/10.5281/zenodo.4764652).

    https://doi.org/10.1111/1755-0998.13597
  • 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
  • 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
  • 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
  • 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 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
  • 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
  • Molecular Ecology
    2016

    Evidence from Pyrosequencing Indicates that Natural Variation in Animal Personality is Associated with DRD4 DNA Methylation

    Eveline Verhulst, A.C. Mateman, M.V. Zwier, Samuel P. Caro, Koen Verhoeven, Kees van Oers
    Personality traits are heritable and respond to natural selection, but are at the same time influenced by the ontogenetic environment. Epigenetic effects, such as DNA methylation, have been proposed as a key mechanism to control personality variation. However, to date little is known about the contribution of epigenetic effects to natural variation in behaviour. Here, we show that great tit (Parus major) lines artificially selected for divergent exploratory behaviour for four generations differ in their DNA methylation levels at the dopamine receptor D4 (DRD4) gene. This D4 receptor is statistically associated with personality traits in both humans and nonhuman animals, including the great tit. Previous work in this songbird failed to detect functional genetic polymorphisms within DRD4 that could account for the gene–trait association. However, our observation supports the idea that DRD4 is functionally involved in exploratory behaviour but that its effects are mediated by DNA methylation. While the exact mechanism underlying the transgenerational consistency of DRD4 methylation remains to be elucidated, this study shows that epigenetic mechanisms are involved in shaping natural variation in personality traits. We outline how this first finding provides a basis for investigating the epigenetic contribution to personality traits in natural systems and its subsequent role for understanding the ecology and evolution of behavioural consistency.
    https://doi.org/10.1111/mec.13519
  • Functional Ecology
    2015

    Costs of sleeping in: circadian rhythms influence cuckoldry risk in a songbird

    Timothy J. Greives, Sjouke A. kingma, Bart Kranstauber, Kim G. Mortega, Martin Wikelski, Kees van Oers, A.C. Mateman, Glen A. Ferguson, Giulia Beltrami, M. Hau
    Circadian (i.e. daily) regulation of behaviors is thought to provide fitness benefits to organisms by enabling them to anticipate diel changes in the environment, such as sunrise. A common behavior among socially monogamous songbirds that usually takes place in the early mornings is copulating with partners outside of the social pair bond (i.e., extra-pair mating). Thus, variation in when individuals begin their daily activity may influence their reproductive success; early risers may be better able to gain copulations and be able to guard their partners and minimize their risk of being cuckolded compared to late risers. Sexual selection may thus play an important role in shaping circadian behaviors, but this assumption has yet to be tested in free-living animals. Here we experimentally weakened endogenous circadian rhythmicity and thus anticipation of dawn in male great tits (Parus major) in the wild through the subcutaneous administration of an implants filled with melatonin shortly before egg-laying began in this population. Selection, particularly sexual selection, may shape circadian phenotypes of wild vertebrates which enable anticipation of important and predictive diel changes in an individuals biotic and abiotic environment.
    https://doi.org/10.1111/1365-2435.12440
  • 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
  • PLoS One
    2014

    Transfer of maternal antibodies against avian influenza virus in mallards (Anas platyrhynchos)

    Jacintha G.B. Van Dijk, A.C. Mateman, M.R.J. Klaassen
    Maternal antibodies protect chicks from infection with pathogens early in life and may impact pathogen dynamics due to the alteration of the proportion of susceptible individuals in a population. We investigated the transfer of maternal antibodies against avian influenza virus (AIV) in a key AIV host species, the mallard (Anas platyrhynchos). Combining observations in both the field and in mallards kept in captivity, we connected maternal AIV antibody concentrations in eggs to (i) female body condition, (ii) female AIV antibody concentration, (iii) egg laying order, (iv) egg size and (v) embryo sex. We applied maternity analysis to the eggs collected in the field to account for intraspecific nest parasitism, which is reportedly high in Anseriformes, detecting parasitic eggs in one out of eight clutches. AIV antibody prevalence in free-living and captive females was respectively 48% and 56%, with 43% and 24% of the eggs receiving these antibodies maternally. In both field and captive study, maternal AIV antibody concentrations in egg yolk correlated positively with circulating AIV antibody concentrations in females. In the captive study, yolk AIV antibody concentrations correlated positively with egg laying order. Female body mass and egg size from the field and captive study, and embryos sex from the field study were not associated with maternal AIV antibody concentrations in eggs. Our study indicates that maternal AIV antibody transfer may potentially play an important role in shaping AIV infection dynamics in mallards.
    https://doi.org/10.1371/journal.pone.0112595
  • Journal of Avian Biology
    2013

    Parental care and UV coloration in blue tits: opposite correlations in males and females between provisioning rate and mate’s coloration

    T. Limbourg, A.C. Mateman, Kate Lessells
    Parental investment and sexually-selected signals can be intimately related, either because the signals indicate the amount of investment that an individual is prepared to make, and hence its value as a mate (the ‘good parent process’), or because individuals are selected to vary their own investment in relation to their mate’s signals (‘differential allocation’ or ‘reproductive compensation’). Correlations between parental investment and the sexually selected signals of both an individual and its mate are therefore of central interest in sexual selection. Blue tits Cyanistes caeruleus are an ideal study species to investigate such correlations because they provide substantial amounts of biparental care and possess sexually-selected structural UV coloration that seems to signal attractiveness in both sexes. We investigated whether feeding rates of male and female blue tits were correlated with either their own or their mate’s UV coloration, and whether any such correlation was affected by the sex ratio of the brood. We also investigated whether any such correlations were reflected in offspring phenotype. Feeding rates were not correlated with either sex of parent’s own UV coloration. However, they were correlated with the mate’s UV coloration, but in opposite directions in males and females: females had higher feeding rates when mated to bright UV males, implying differential allocation, while males had lower feeding rates when mated to bright UV females, implying reproductive compensation. These relationships were unaffected by the sex ratio of the brood. In addition, fledgling tarsus length, but not mass, was related to male UV coloration, and to female UV coloration in interaction with male age. These results suggest that both male and female attractiveness influence parental investment of the mate, and that this in turn affects offspring phenotype. We found no evidence for differential sex allocation.
    https://doi.org/10.1111/j.1600-048X.2012.05575.x
  • Biology Letters
    2013

    Opposite differential allocation by males and females of the same species

    T. Limbourg, A.C. Mateman, Kate Lessells
    Differential allocation (DA)—the adjustment of an individual’s parental investment in relation to its mate’s attractiveness—is increasingly recognized as an important component of sexual selection. However, although DA is expected by both sexes of parents in species with biparental care, DA by males has rarely been investigated. We have previously demonstrated a decrease in the feeding rates of female blue tits Cyanistes caeruleus when their mate’s UV coloration was experimentally reduced (i.e. positive DA). In this study, we used the same experimental protocol in the same population to investigate DA by male blue tits in relation to their female’s UV coloration. Males mated to UV-reduced females had higher feeding rates than those mated to control females (i.e. negative DA). Thus, male and female blue tits display opposite DA for the same component of parental effort (chick provisioning), the first time that this has been reported for any species.
    https://doi.org/10.1098/rsbl.2012.0835
  • 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
  • Ostrich
    2011

    An additional field method to sex adult Barn Swallows during the non-breeding season in Zambia: white spot length in the outer tail feather

    S. Duijns, Jacintha G.B. Van Dijk, R.H.S. Kraus, A.C. Mateman, B. van den Brink, P. Van Hooft
    Adult Barn Swallows Hirundo rustica exhibit strong sexual size dimorphism in the length of the outermost tail feathers, which are longer in males compared with females. This trait is traditionally used to sex adult Barn Swallows in the field. However, due to the wear and breakage of the tips of the outer tail feather and tail moult during the non-breeding season, sexing becomes unreliable or even impossible. We therefore tested whether the length of the white spot on the outer tail feather is sexually dimorphic, and whether it can be used as an additional sexing method for adult Barn Swallows. The white spot length was sexually dimorphic, based on DNA analysis of 101 adult individuals caught at their roost during the non-breeding season in Zambia. Accuracy in sex determination of 95% could be obtained by classifying individuals with a white spot length 29.5 mm as males. When applying the length of the white spot as an additional method to sex adult Barn Swallows on all birds caught in Zambia during the study period (N = 759), the percentage of birds that could successfully be sexed increased to more than 55%. Therefore we emphasise the importance of measuring the white spot length in addition to the tail fork depth and tail length to sex adult Barn Swallows in the non-breeding season.
    https://doi.org/10.2989/00306525.2011.603467

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