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Martin Bulla

Max Planck Institut für Ornithologie, Department of Behavioural Ecology & Evolutionary Genetics, Graduate Student

Royal Netherlands Institute for Sea Research, Departmnent of Coastal Systems, Post-Doc

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Behavioural ecologists and ornithologists curious about biorhythms, especially those found in the wild and during reproduction. Passionate about the shorebirds and Arctic.
Supervisors: Bart Kempenaers, Theunis Piersma, Mihai Valcu, Barbara Helm, Anne Rutten, and Miroslav Šálek
Phone: +49 (0)8157-932-264
Address: Department of Behavioural Ecology & Evolutionary Genetics
Max Planck Institute for Ornithology
Eberhard-Gwinner-Strasse 7
82319 Seewiesen, Germany

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Papers by Martin Bulla

Same data, different analysts: variation in effect sizes due to analytical decisions in ecology and evolutionary biology

Although variation in effect sizes and predicted values among studies of similar phenomena is ine... more Although variation in effect sizes and predicted values among studies of similar phenomena is inevitable, such variation far exceeds what might be produced by sampling error alone. One possible explanation for variation among results is differences among researchers in the decisions they make regarding statistical analyses. A growing array of studies has explored this analytical variability in different (mostly social science) fields, and has found substantial variability among results, despite analysts having the same data and research question. We implemented an analogous study in ecology and evolutionary biology, fields in which there have been no empirical exploration of the variation in effect sizes or model predictions generated by the analytical decisions of different researchers. We used two unpublished datasets, one from evolutionary ecology (blue tit, Cyanistes caeruleus, to compare sibling number and nestling growth) and one from conservation ecology (Eucalyptus, to compa...

Marine biorhythms: bridging chronobiology and ecology

Philosophical Transactions of the Royal Society B, Oct 9, 2017

One contribution of 12 to a theme issue 'Wild clocks: integrating chronobiology and ecology to un... more

Supporting information for 'Diversity of incubation rhythms in a facultatively uniparental shorebird – the Northern Lapwing

Methods in field chronobiology

Philosophical Transactions of the Royal Society B, Oct 9, 2017

One contribution of 12 to a theme issue 'Wild clocks: integrating chronobiology and ecology to un... more

Marketing and non‐profit organizations in the Czech Republic

European Journal of Marketing, 2006

Objectives: Smoking is the leading cause of premature mortality and morbidity. The aim of this st... more Objectives: Smoking is the leading cause of premature mortality and morbidity. The aim of this study was to provide the first national description of organizational capacity and involvement in tobacco control (TC) measures outlined by the WHO Framework Convention on Tobacco Control (FCTC) within the Czech Republic. Methods: Data were collected in a national cross-sectional survey of all 14 organizations engaged in TC activities within the Czech Republic. Organizational capacity (defined as skills, supports, partnerships, resources, and leadership) to implement TC activities, and level of involvement in key FCTC measures were assessed and compared across organizations. Results: Despite the high economic costs of tobacco use, few organizations were involved in TC activities. 50% of all organizations involved in TC activities were non-government or non-profit organizations. Less than one third of organizations reported having a sufficient number of staff or adequate funding to work effectively. Skills for chronic disease prevention (CDP) practice including assessment, identifying relevant practices, developing and implementing initiatives were rated more favourably than skills to evaluate these activities. Level of involvement was ranked highest for activities that focused on creation of smoke-free environments and lowest for activities that focused on raising taxes and sales to minors. Organizations tended to be more involved in individual, rather than population-level prevention strategies. Inadequate funding, insufficient number of staff dedicated to working on TC, and lack of political will were major barriers. Conclusions: This paper provides the first national description of organizational capacity and level of involvement in FCTC measures within the Czech Republic.

Scrutinizing assortative mating in birds

PLOS Biology, Feb 21, 2019

It is often claimed that pair bonds preferentially form between individuals that resemble one ano... more It is often claimed that pair bonds preferentially form between individuals that resemble one another. Such assortative mating appears to be widespread throughout the animal kingdom. Yet it is unclear whether the apparent ubiquity of assortative mating arises primarily from mate choice ("like attracts like"), which can be constrained by same-sex competition for mates; from spatial or temporal separation; or from observer, reporting, publication, or search bias. Here, based on a conventional literature search, we find compelling meta-analytical evidence for size-assortative mating in birds (r = 0.178, 95% CI 0.142-0.215, 83 species, 35,591 pairs). However, our analyses reveal that this effect vanishes gradually with increased control of confounding factors. Specifically, the effect size decreased by 42% when we used previously unpublished data from nine long-term field studies, i.e., data free of reporting and publication bias (r = 0.103, 95% CI 0.074-0.132, eight species, 16,611 pairs). Moreover, in those data, assortative mating effectively disappeared when both partners were measured by independent observers or separately in space and time (mean r = 0.018, 95% CI −0.016-0.057). Likewise, we also found no evidence for assortative mating in a direct experimental test for mutual mate choice in captive populations of Zebra finches (r = −0.020, 95% CI −0.148-0.107, 1,414 pairs). These results highlight the importance of unpublished data in generating unbiased meta-analytical conclusions and suggest that the apparent ubiquity of assortative mating reported in the literature is overestimated and may not be driven by mate choice or mating competition for preferred mates.

Biparental incubation-scheduling: no experimental evidence for major energetic constraints

Behavioral Ecology, Sep 3, 2014

Incubation is energetically demanding, but it is debated whether these demands constrain incubati... more Incubation is energetically demanding, but it is debated whether these demands constrain incubation-scheduling (i.e., the length, constancy, and timing of incubation bouts) in cases where both parents incubate. Using 2 methods, we experimentally reduced the energetic demands of incubation in the semipalmated sandpiper, a biparental shorebird breeding in the harsh conditions of the high Arctic. First, we decreased the demands of incubation for 1 parent only by exchanging 1 of the 4 eggs for an artificial egg that heated up when the focal bird incubated. Second, we reanalyzed the data from the only published experimental study that has explicitly tested energetic constraints on incubation-scheduling in a biparentally incubating species (Cresswell et al. 2003). In this experiment, the energetic demands of incubation were decreased for both parents by insulating the nest cup. We expected that the treated birds, in both experiments, would change the length of their incubation bouts, if biparental incubation-scheduling is energetically constrained. However, we found no evidence that heating or insulation of the nest affected the length of incubation bouts: the combined effect of both experiments was an increase in bout length of 3.6 min (95% CI: −33 to 40), which is equivalent to a 0.5% increase in the length of the average incubation bout. These results demonstrate that the observed biparental incubation-scheduling in semipalmated sandpipers is not primarily driven by energetic constraints and therefore by the state of the incubating bird, implying that we still do not understand the factors driving biparental incubation-scheduling.

Diverse incubation rhythms in a facultatively uniparental shorebird – the Northern Lapwing

bioRxiv (Cold Spring Harbor Laboratory), May 17, 2018

Incubation by both parents is the most common form of care for eggs. Although the involvement of ... more Incubation by both parents is the most common form of care for eggs. Although the involvement of the two parents may vary dramatically between and within pairs, as well as over the day and breeding season, detailed description of this variation (especially in species with variable male contribution to incubation) is rare. Here, we continuously video-monitored 113 nests of Northern Lapwing Vanellus vanellus over the breeding season to reveal the diversity of incubation rhythms and parental involvement. We found great between-nest variation in the overall nest attendance (68-94%; median = 87%) and in how much males incubated (0-37%; median = 13%). Notably, the less the males incubated, the lower was the overall nest attendance, even though females partially compensated for the males' decrease. Overall, incubation rhythms changed little over the season and incubation period. However, as nights shorten with the progressing breeding season, the female longest night incubation bout shortened too. Essentially, nest attendance was highest, incubation bouts longest, exchange gaps shortest and male involvement lowest during the night. Also, males tended to incubate the most after sunrise and before sunset. To conclude, we revealed strong circadian rhythms and remarkable between nest differences in Northern Lapwing incubation (especially in male involvement), yet despite seasonal environmental trends (e.g. increasing temperature) Lapwing incubation rhythms remained relatively stable over the season and incubation period. .

Behavioural rhythms and parental cooperation in biparentally incubating shorebirds

All organisms exhibit alternating phases of different behaviours. These behavioural rhythms are t... more All organisms exhibit alternating phases of different behaviours. These behavioural rhythms are thought to be under strong selection, influenced by the rhythmicity of the environment. Whereas behavioural rhythms are well studied in isolated individuals under laboratory conditions, in free-living populations, individuals have to temporally synchronize their activities with those of others. The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological factors that shape them remain poorly understood. Here, we address this issue for biparental care-a complex social behaviour and a particularly sensitive phase of social synchronization-in which pair members potentially compromise their individual rhythms. We use non-model organisms-biparentallyincubating shorebirds-where parents synchronize to achieve continuous coverage of developing eggs, and we use an array of monitoring techniques to record incubation in the wild. We combine a within-species approach (i.e. detailed description of incubation rhythms and field experiments to reveal the drivers of the rhythms using a single species; Chapter 1-3 & 5), with a between-species approach (i.e. comparing incubation rhythms of biparental and uniparental species; Chapter 4), and a phylogenetically informed comparative analyses (i.e. descriptive and hypotheses driven analyses across shorebirds; Chapter 6). Specifically, we tested: (1) how parents share their incubation duties over the day, incubation period and season (Chapter 1), and whether incubation behaviour correlates with off-nest behaviour (Chapter 2); (2) whether incubating parents compensate for the absence of their partner's care (Chapter 3); (3) whether a complete switch to uniparental incubation is possible (Chapter 4); (4) whether energetic demands of incubation constrain incubation rhythms (Chapter 5 & 6); and finally (5), whether the diversity in incubation rhythms relates to phylogeny, predation risk, energetics and environmental fluctuations (Chapter 6). We first found-in a high Arctic breeding shorebird, the semipalmated sandpiper, Calidris pusilla (Chapter 1)-that overall the daily timing of incubation shifted over the incubation period (i.e. in females from evening-night to night-morning incubation) and over the season. However, the timing varied considerably among pairs: some displayed day-night incubation rhythm, others free-running like incubation rhythm (i.e. pairs shifted the start of incubation bouts between days so that each parent experienced similar conditions across the incubation period). Off-nest behaviour of the semipalmated sandpiper parents varied between sexes, across time and weather conditions, but it did not explain the diverse incubation rhythms (Chapter 2). We later confirmed this lack of evidence for energetic constraint of incubation in a field experiment (Chapter 5) and via comparative analyses (Chapter 6). Off duty parents roamed on average 224 m from their nest, implying that direct S u m m a r y | iii communication with the incubating partner is unlikely (Chapter 2). These results suggest that parents communicate only during their brief exchange on the nest. Second, despite this lack of communication between parents, overall, the parents partially compensated for an experimentally-induced temporary absence of their partner's care (Chapter 3). However, the individual responses span the entire range of what is possible (no, partial and full compensation). Whether some parents may lack the energy for full compensation, or are less responsive to their partner's absence, is unclear; however, we provide tentative evidence for both. Essentially, since incubating parents do not feed, even the fully compensating parents later left their nest unattended. Nevertheless, where removed parent never returned, nests were incubated uniparentally for median of 4 days (range 0-10 days, N = 7 nests). Third, we found natural cases of such uniparental incubating in 8 out of 15 biparentally incubating shorebird-species (Chapter 4). Such uniparental incubation resembled the incubation of uniparental species. Strikingly, in 5 species we document cases where uniparentally incubating parents brought their clutch to hatching, which in these species reveals a potential for a flexible switch from biparental to uniparental care. Fourth, contrary to prior believe, reducing the energetic demands of incubation by heating or insulating the nest cup had no effect on the length of incubation bouts (Chapter 5). These results convincingly demonstrate that incubation rhythms in semipalmated sandpipers are not primarily driven by the energetic state of the incubating bird. Last, in a large scale comparative study that made use of 729 nests from 91 populations of 32 species we found a remarkable within-and between-species diversity in the socially synchronized incubation rhythms (Chapter 6). The length of incubation bouts was unrelated to variables reflecting energetic demands, but species relying on crypsis had longer incubation bouts than those that are readily visible or actively protect their nest against predators. Rhythms that could be potentially entrained to the 24-h light-dark cycle were less likely at high latitudes and absent in 18 species. Although half of our species are tidal away from their breeding grounds, and some forage in tidal areas also during breeding, in only 5% of nests did pairs display a rhythm that can be entrained by the tide. Hence, unlike the 24-h light-dark cycle, tidal life-history seems to play, at best, a negligible role in determining incubation rhythms. In sum, we reveal unexpected within-and between-species diversity in socially synchronized incubation rhythms of biparental shorebirds (Chapter 1, 3, 4, & 6). Our results demonstrate that under natural conditions social synchronization can generate much more diverse rhythms than previously expected, and that these rhythms often defy the 24-h day, even in day-night environments (Chapter 6). Whereas our descriptive, experimental and comparative evidence consistently rules out risk of starvation as a key factor underlying the diversity and timing of these rhythms (Chapter 2, 5 & 6), we provide novel evidence for the link between the diversity of the rhythms and anti-predation strategy (Chapter 6). 2 | B e h a v i o u r a l r h y t h m s i n i n c u b a t i n g s h o r e b i r d s Social synchronization Behavioural rhythms of individuals are not only synchronized by the environmental cycles, but are also shaped by the social environment-including potential mates, allies, competitors, prey, or predators (Mrosovsky 1996; Davidson & Menaker 2003; Mistlberger & Skene 2004; Castillo-Ruiz et al. 2012; Bloch et al. 2013). As a result of such social interactions, individuals can temporally segregate their daily activities (e.g. prey avoiding predators, subordinates avoiding dominants), or synchronize their activities (e.g. foraging in group, communal defence against predators, pairs reproducing or caring for offspring;

Sperm traits of the three genetic morphs in the ruff sandpiper

bioRxiv (Cold Spring Harbor Laboratory), Jul 30, 2023

The ruff sandpiper Calidris pugnax is a Palearctic lekking shorebird with three genetic morphs de... more The ruff sandpiper Calidris pugnax is a Palearctic lekking shorebird with three genetic morphs determined by an autosomal inversion. Male morphs differ strikingly in body size, ornaments, endocrinology and mating behavior. Aggressive Independents represent the ancestral haplotype, semicooperative Satellites and female-mimicking Faeders the inverted haplotypes. Since one inversion breakpoint is homozygous lethal, the inverted haplotypes (Satellite and Faeder) cannot recombine and are expected to accumulate mutations. The inversion regions also harbor genes involved in spermatogenesis. However, it is unknown whether the genetic difference between the morphs also translate into differences in sperm traits. Here, we use a captive-bred population of ruffs to compare sperm velocity and morphology among the morphs. Faeder sperm moved the slowest, which is in line with expectations from mutation accumulation and the idea that Faeders might fare worse than Satellites, as Satellite haplotype arose through a rare recombination event that may have reinstated the function of sperm-related genes or helped to purge deleterious mutations. Against the expectation from mutation accumulation, sperm of Independents did not seem to be of highest quality, i.e., they were not the fastest nor the least variable, and they had the shortest tail and midpiece. Although the midpiece contains the energy-producing mitochondria, sperm midpiece length was not associated with sperm swimming speed. Instead, two of three velocity metrics were weakly positively associated with head length (absolute and relative). These results may relate to our observation that although ruff sperm morphologically resemble those of passerines, they generally appear to move differently, vibrating from side to side while slowly moving forward, rather than rotating while moving forwards. To conclude, the three genetically determined morphs showed only minor differences in sperm traits, and these differences were not clearly associated with variation in sperm velocity, indicating a low potential for the evolution of morph-specific sperm adaptations. .

Urban birds’ flight responses were unaffected by the COVID-19 shutdowns

The coronavirus disease 2019 (COVID-19) pandemic has dramatically altered human activities, poten... more The coronavirus disease 2019 (COVID-19) pandemic has dramatically altered human activities, potentially relieving human pressures on urban-dwelling animals. Here, we evaluated whether birds from five cities in five countries (Czech Republic – Prague, Finland – Rovaniemi, Hungary – Budapest, Poland – Poznan, and Australia – Melbourne) changed their tolerance towards human presence (measured as flight initiation distance) during the COVID-19 shutdowns. We collected 6369 flight initiation distance estimates for 147 bird species and found that birds tolerated approaching humans to a similar level before and during the COVID-19 shutdowns. Moreover, during the shutdowns, bird escape behaviour did not consistently change with the level of governmental restrictions (measured as the stringency index). Hence, our results indicate that birds do not flexibly and quickly adjust their escape behaviour to the reduced human presence; in other words, the breeding populations of urban birds examined ...

PRISMA_literature summary

The process of literature investigation

Diversity of incubation rhythms in a facultatively uniparental shorebird – the Northern Lapwing

Scientific Reports, Mar 18, 2019

Lapwing population, nest attendance highly correlates with actual incubation (warming or shading ... more Lapwing population, nest attendance highly correlates with actual incubation (warming or shading of eggs 13,24,32 ; Supplementary actograms 33). Also, females and males seem to heat the cutch to the similar temperatures (13,24,32,34 ; Supplementary actograms 33). We specifically investigated (1) between-nest variation in overall nest attendance (proportion of observed time parents were sitting on the nest or shading the eggs), (2) how male nest attendance relates to this between-nest variation in nest attendance, as a single parent cannot incubate with high nest attendance indefinitely, and (3) tested how incubation rhythm (female and male contribution) changed within a day, throughout the incubation period and season as food availability 35,36 , temperature and predation pressure 37,38 , as well as brood value vary over temporal time scales 39-41. Results overall nest attendance. Northern Lapwing parents incubated their eggs 87% of time (median, range: 68-94%, N = 60 nests with more than 2 days of recording; Fig. 1a, dark red and blue). Actual incubation bouts, defined as the time between the arrival of a parent at the nest and its departure, followed by the incubation of its partner (i.e. the total time allocated to a single parent including incubation recesses), covered 98% of observed time (median, range: 95-100%, N = 55 nests incubated by both parents; Fig. 1a, red and blue). In other words,

Sperm traits of the three genetic morphs in the ruff sandpiper

The ruff sandpiperCalidris pugnaxis a Palearctic lekking shorebird with three genetic morphs dete... more The ruff sandpiperCalidris pugnaxis a Palearctic lekking shorebird with three genetic morphs determined by an autosomal inversion. Male morphs differ strikingly in body size, ornaments, endocrinology and mating behavior. Aggressive Independents represent the ancestral haplotype, semi-cooperative Satellites and female-mimicking Faeders the inverted haplotypes. Since one inversion breakpoint is homozygous lethal, the inverted haplotypes (Satellite and Faeder) cannot recombine and are expected to accumulate mutations. The inversion regions also harbor genes involved in spermatogenesis. However, it is unknown whether the genetic difference between the morphs also translate into differences in sperm traits. Here, we use a captive-bred population of ruffs to compare sperm velocity and morphology among the morphs. Faeder sperm moved the slowest, which is in line with expectations from mutation accumulation and the idea that Faeders might fare worse than Satellites, as Satellite haplotype a...

Supporting information for 'Nest relief in the cryptically incubating semipalmated sandpiper is quick, but vocal

OSF, Sep 2, 2019

Supporting information for 'Diel timing of nest predation changes across breeding season in a subtropical shorebird

The data supporting the results, computer code used to generate the results, and the Supplementar... more

S5_Data_xlsx

Data for Fig 1B: Strength of assortative mating for size as a function of data source

S3_Data.xlsx

Unpublished data (nine long-term field studies): Data where we combined the information from data... more

Datasets

DATASET

Data from: Biparental incubation patterns in a high-Arctic breeding shorebird: how do pairs divide their duties?

In biparental species, parents may be in conflict over how much they invest into their offspring.... more In biparental species, parents may be in conflict over how much they invest into their offspring. To understand this conflict, parental care needs to be accurately measured, something rarely done. Here, we quantitatively describe the outcome of parental conflict in terms of quality, amount and timing of incubation throughout the 21 day incubation period in a population of semipalmated sandpipers (Calidris pusilla) breeding under continuous daylight in the High Arctic. Incubation quality, measured by egg temperature and incubation constancy, showed no marked difference between the sexes. The amount of incubation, measured as length of incubation bouts, was on average 51 min longer per bout for females (11.5 h) than for males (10.7 h), at first glance suggesting that females invested more than males. However, this difference may have been offset by sex-differences in the timing of incubation; females were more often off-nest during the warmer period of the day, when foraging conditions were presumably better. Overall, the daily timing of incubation shifted over the incubation period (e. g., for female incubation from ‘evening-night’ to ‘night-morning’) and over the season, but varied considerably among pairs. At one extreme, pairs shared the amount of incubation equally, but one parent always incubated during the colder part of the day; at the other extreme, pairs shifted the start of incubation bouts between days so that each parent experienced similar conditions across the incubation period. Our results highlight how the simultaneous consideration of different aspects of care across time allows sex-specific investment to be more accurately quantified

Same data, different analysts: variation in effect sizes due to analytical decisions in ecology and evolutionary biology

Although variation in effect sizes and predicted values among studies of similar phenomena is ine... more Although variation in effect sizes and predicted values among studies of similar phenomena is inevitable, such variation far exceeds what might be produced by sampling error alone. One possible explanation for variation among results is differences among researchers in the decisions they make regarding statistical analyses. A growing array of studies has explored this analytical variability in different (mostly social science) fields, and has found substantial variability among results, despite analysts having the same data and research question. We implemented an analogous study in ecology and evolutionary biology, fields in which there have been no empirical exploration of the variation in effect sizes or model predictions generated by the analytical decisions of different researchers. We used two unpublished datasets, one from evolutionary ecology (blue tit, Cyanistes caeruleus, to compare sibling number and nestling growth) and one from conservation ecology (Eucalyptus, to compa...

Marine biorhythms: bridging chronobiology and ecology

Philosophical Transactions of the Royal Society B, Oct 9, 2017

One contribution of 12 to a theme issue 'Wild clocks: integrating chronobiology and ecology to un... more

Supporting information for 'Diversity of incubation rhythms in a facultatively uniparental shorebird – the Northern Lapwing

Methods in field chronobiology

Philosophical Transactions of the Royal Society B, Oct 9, 2017

One contribution of 12 to a theme issue 'Wild clocks: integrating chronobiology and ecology to un... more

Marketing and non‐profit organizations in the Czech Republic

European Journal of Marketing, 2006

Objectives: Smoking is the leading cause of premature mortality and morbidity. The aim of this st... more Objectives: Smoking is the leading cause of premature mortality and morbidity. The aim of this study was to provide the first national description of organizational capacity and involvement in tobacco control (TC) measures outlined by the WHO Framework Convention on Tobacco Control (FCTC) within the Czech Republic. Methods: Data were collected in a national cross-sectional survey of all 14 organizations engaged in TC activities within the Czech Republic. Organizational capacity (defined as skills, supports, partnerships, resources, and leadership) to implement TC activities, and level of involvement in key FCTC measures were assessed and compared across organizations. Results: Despite the high economic costs of tobacco use, few organizations were involved in TC activities. 50% of all organizations involved in TC activities were non-government or non-profit organizations. Less than one third of organizations reported having a sufficient number of staff or adequate funding to work effectively. Skills for chronic disease prevention (CDP) practice including assessment, identifying relevant practices, developing and implementing initiatives were rated more favourably than skills to evaluate these activities. Level of involvement was ranked highest for activities that focused on creation of smoke-free environments and lowest for activities that focused on raising taxes and sales to minors. Organizations tended to be more involved in individual, rather than population-level prevention strategies. Inadequate funding, insufficient number of staff dedicated to working on TC, and lack of political will were major barriers. Conclusions: This paper provides the first national description of organizational capacity and level of involvement in FCTC measures within the Czech Republic.

Scrutinizing assortative mating in birds

PLOS Biology, Feb 21, 2019

It is often claimed that pair bonds preferentially form between individuals that resemble one ano... more It is often claimed that pair bonds preferentially form between individuals that resemble one another. Such assortative mating appears to be widespread throughout the animal kingdom. Yet it is unclear whether the apparent ubiquity of assortative mating arises primarily from mate choice ("like attracts like"), which can be constrained by same-sex competition for mates; from spatial or temporal separation; or from observer, reporting, publication, or search bias. Here, based on a conventional literature search, we find compelling meta-analytical evidence for size-assortative mating in birds (r = 0.178, 95% CI 0.142-0.215, 83 species, 35,591 pairs). However, our analyses reveal that this effect vanishes gradually with increased control of confounding factors. Specifically, the effect size decreased by 42% when we used previously unpublished data from nine long-term field studies, i.e., data free of reporting and publication bias (r = 0.103, 95% CI 0.074-0.132, eight species, 16,611 pairs). Moreover, in those data, assortative mating effectively disappeared when both partners were measured by independent observers or separately in space and time (mean r = 0.018, 95% CI −0.016-0.057). Likewise, we also found no evidence for assortative mating in a direct experimental test for mutual mate choice in captive populations of Zebra finches (r = −0.020, 95% CI −0.148-0.107, 1,414 pairs). These results highlight the importance of unpublished data in generating unbiased meta-analytical conclusions and suggest that the apparent ubiquity of assortative mating reported in the literature is overestimated and may not be driven by mate choice or mating competition for preferred mates.

Biparental incubation-scheduling: no experimental evidence for major energetic constraints

Behavioral Ecology, Sep 3, 2014

Incubation is energetically demanding, but it is debated whether these demands constrain incubati... more Incubation is energetically demanding, but it is debated whether these demands constrain incubation-scheduling (i.e., the length, constancy, and timing of incubation bouts) in cases where both parents incubate. Using 2 methods, we experimentally reduced the energetic demands of incubation in the semipalmated sandpiper, a biparental shorebird breeding in the harsh conditions of the high Arctic. First, we decreased the demands of incubation for 1 parent only by exchanging 1 of the 4 eggs for an artificial egg that heated up when the focal bird incubated. Second, we reanalyzed the data from the only published experimental study that has explicitly tested energetic constraints on incubation-scheduling in a biparentally incubating species (Cresswell et al. 2003). In this experiment, the energetic demands of incubation were decreased for both parents by insulating the nest cup. We expected that the treated birds, in both experiments, would change the length of their incubation bouts, if biparental incubation-scheduling is energetically constrained. However, we found no evidence that heating or insulation of the nest affected the length of incubation bouts: the combined effect of both experiments was an increase in bout length of 3.6 min (95% CI: −33 to 40), which is equivalent to a 0.5% increase in the length of the average incubation bout. These results demonstrate that the observed biparental incubation-scheduling in semipalmated sandpipers is not primarily driven by energetic constraints and therefore by the state of the incubating bird, implying that we still do not understand the factors driving biparental incubation-scheduling.

Diverse incubation rhythms in a facultatively uniparental shorebird – the Northern Lapwing

bioRxiv (Cold Spring Harbor Laboratory), May 17, 2018

Incubation by both parents is the most common form of care for eggs. Although the involvement of ... more Incubation by both parents is the most common form of care for eggs. Although the involvement of the two parents may vary dramatically between and within pairs, as well as over the day and breeding season, detailed description of this variation (especially in species with variable male contribution to incubation) is rare. Here, we continuously video-monitored 113 nests of Northern Lapwing Vanellus vanellus over the breeding season to reveal the diversity of incubation rhythms and parental involvement. We found great between-nest variation in the overall nest attendance (68-94%; median = 87%) and in how much males incubated (0-37%; median = 13%). Notably, the less the males incubated, the lower was the overall nest attendance, even though females partially compensated for the males' decrease. Overall, incubation rhythms changed little over the season and incubation period. However, as nights shorten with the progressing breeding season, the female longest night incubation bout shortened too. Essentially, nest attendance was highest, incubation bouts longest, exchange gaps shortest and male involvement lowest during the night. Also, males tended to incubate the most after sunrise and before sunset. To conclude, we revealed strong circadian rhythms and remarkable between nest differences in Northern Lapwing incubation (especially in male involvement), yet despite seasonal environmental trends (e.g. increasing temperature) Lapwing incubation rhythms remained relatively stable over the season and incubation period. .

Behavioural rhythms and parental cooperation in biparentally incubating shorebirds

All organisms exhibit alternating phases of different behaviours. These behavioural rhythms are t... more All organisms exhibit alternating phases of different behaviours. These behavioural rhythms are thought to be under strong selection, influenced by the rhythmicity of the environment. Whereas behavioural rhythms are well studied in isolated individuals under laboratory conditions, in free-living populations, individuals have to temporally synchronize their activities with those of others. The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological factors that shape them remain poorly understood. Here, we address this issue for biparental care-a complex social behaviour and a particularly sensitive phase of social synchronization-in which pair members potentially compromise their individual rhythms. We use non-model organisms-biparentallyincubating shorebirds-where parents synchronize to achieve continuous coverage of developing eggs, and we use an array of monitoring techniques to record incubation in the wild. We combine a within-species approach (i.e. detailed description of incubation rhythms and field experiments to reveal the drivers of the rhythms using a single species; Chapter 1-3 & 5), with a between-species approach (i.e. comparing incubation rhythms of biparental and uniparental species; Chapter 4), and a phylogenetically informed comparative analyses (i.e. descriptive and hypotheses driven analyses across shorebirds; Chapter 6). Specifically, we tested: (1) how parents share their incubation duties over the day, incubation period and season (Chapter 1), and whether incubation behaviour correlates with off-nest behaviour (Chapter 2); (2) whether incubating parents compensate for the absence of their partner's care (Chapter 3); (3) whether a complete switch to uniparental incubation is possible (Chapter 4); (4) whether energetic demands of incubation constrain incubation rhythms (Chapter 5 & 6); and finally (5), whether the diversity in incubation rhythms relates to phylogeny, predation risk, energetics and environmental fluctuations (Chapter 6). We first found-in a high Arctic breeding shorebird, the semipalmated sandpiper, Calidris pusilla (Chapter 1)-that overall the daily timing of incubation shifted over the incubation period (i.e. in females from evening-night to night-morning incubation) and over the season. However, the timing varied considerably among pairs: some displayed day-night incubation rhythm, others free-running like incubation rhythm (i.e. pairs shifted the start of incubation bouts between days so that each parent experienced similar conditions across the incubation period). Off-nest behaviour of the semipalmated sandpiper parents varied between sexes, across time and weather conditions, but it did not explain the diverse incubation rhythms (Chapter 2). We later confirmed this lack of evidence for energetic constraint of incubation in a field experiment (Chapter 5) and via comparative analyses (Chapter 6). Off duty parents roamed on average 224 m from their nest, implying that direct S u m m a r y | iii communication with the incubating partner is unlikely (Chapter 2). These results suggest that parents communicate only during their brief exchange on the nest. Second, despite this lack of communication between parents, overall, the parents partially compensated for an experimentally-induced temporary absence of their partner's care (Chapter 3). However, the individual responses span the entire range of what is possible (no, partial and full compensation). Whether some parents may lack the energy for full compensation, or are less responsive to their partner's absence, is unclear; however, we provide tentative evidence for both. Essentially, since incubating parents do not feed, even the fully compensating parents later left their nest unattended. Nevertheless, where removed parent never returned, nests were incubated uniparentally for median of 4 days (range 0-10 days, N = 7 nests). Third, we found natural cases of such uniparental incubating in 8 out of 15 biparentally incubating shorebird-species (Chapter 4). Such uniparental incubation resembled the incubation of uniparental species. Strikingly, in 5 species we document cases where uniparentally incubating parents brought their clutch to hatching, which in these species reveals a potential for a flexible switch from biparental to uniparental care. Fourth, contrary to prior believe, reducing the energetic demands of incubation by heating or insulating the nest cup had no effect on the length of incubation bouts (Chapter 5). These results convincingly demonstrate that incubation rhythms in semipalmated sandpipers are not primarily driven by the energetic state of the incubating bird. Last, in a large scale comparative study that made use of 729 nests from 91 populations of 32 species we found a remarkable within-and between-species diversity in the socially synchronized incubation rhythms (Chapter 6). The length of incubation bouts was unrelated to variables reflecting energetic demands, but species relying on crypsis had longer incubation bouts than those that are readily visible or actively protect their nest against predators. Rhythms that could be potentially entrained to the 24-h light-dark cycle were less likely at high latitudes and absent in 18 species. Although half of our species are tidal away from their breeding grounds, and some forage in tidal areas also during breeding, in only 5% of nests did pairs display a rhythm that can be entrained by the tide. Hence, unlike the 24-h light-dark cycle, tidal life-history seems to play, at best, a negligible role in determining incubation rhythms. In sum, we reveal unexpected within-and between-species diversity in socially synchronized incubation rhythms of biparental shorebirds (Chapter 1, 3, 4, & 6). Our results demonstrate that under natural conditions social synchronization can generate much more diverse rhythms than previously expected, and that these rhythms often defy the 24-h day, even in day-night environments (Chapter 6). Whereas our descriptive, experimental and comparative evidence consistently rules out risk of starvation as a key factor underlying the diversity and timing of these rhythms (Chapter 2, 5 & 6), we provide novel evidence for the link between the diversity of the rhythms and anti-predation strategy (Chapter 6). 2 | B e h a v i o u r a l r h y t h m s i n i n c u b a t i n g s h o r e b i r d s Social synchronization Behavioural rhythms of individuals are not only synchronized by the environmental cycles, but are also shaped by the social environment-including potential mates, allies, competitors, prey, or predators (Mrosovsky 1996; Davidson & Menaker 2003; Mistlberger & Skene 2004; Castillo-Ruiz et al. 2012; Bloch et al. 2013). As a result of such social interactions, individuals can temporally segregate their daily activities (e.g. prey avoiding predators, subordinates avoiding dominants), or synchronize their activities (e.g. foraging in group, communal defence against predators, pairs reproducing or caring for offspring;

Sperm traits of the three genetic morphs in the ruff sandpiper

bioRxiv (Cold Spring Harbor Laboratory), Jul 30, 2023

The ruff sandpiper Calidris pugnax is a Palearctic lekking shorebird with three genetic morphs de... more The ruff sandpiper Calidris pugnax is a Palearctic lekking shorebird with three genetic morphs determined by an autosomal inversion. Male morphs differ strikingly in body size, ornaments, endocrinology and mating behavior. Aggressive Independents represent the ancestral haplotype, semicooperative Satellites and female-mimicking Faeders the inverted haplotypes. Since one inversion breakpoint is homozygous lethal, the inverted haplotypes (Satellite and Faeder) cannot recombine and are expected to accumulate mutations. The inversion regions also harbor genes involved in spermatogenesis. However, it is unknown whether the genetic difference between the morphs also translate into differences in sperm traits. Here, we use a captive-bred population of ruffs to compare sperm velocity and morphology among the morphs. Faeder sperm moved the slowest, which is in line with expectations from mutation accumulation and the idea that Faeders might fare worse than Satellites, as Satellite haplotype arose through a rare recombination event that may have reinstated the function of sperm-related genes or helped to purge deleterious mutations. Against the expectation from mutation accumulation, sperm of Independents did not seem to be of highest quality, i.e., they were not the fastest nor the least variable, and they had the shortest tail and midpiece. Although the midpiece contains the energy-producing mitochondria, sperm midpiece length was not associated with sperm swimming speed. Instead, two of three velocity metrics were weakly positively associated with head length (absolute and relative). These results may relate to our observation that although ruff sperm morphologically resemble those of passerines, they generally appear to move differently, vibrating from side to side while slowly moving forward, rather than rotating while moving forwards. To conclude, the three genetically determined morphs showed only minor differences in sperm traits, and these differences were not clearly associated with variation in sperm velocity, indicating a low potential for the evolution of morph-specific sperm adaptations. .

Urban birds’ flight responses were unaffected by the COVID-19 shutdowns

The coronavirus disease 2019 (COVID-19) pandemic has dramatically altered human activities, poten... more The coronavirus disease 2019 (COVID-19) pandemic has dramatically altered human activities, potentially relieving human pressures on urban-dwelling animals. Here, we evaluated whether birds from five cities in five countries (Czech Republic – Prague, Finland – Rovaniemi, Hungary – Budapest, Poland – Poznan, and Australia – Melbourne) changed their tolerance towards human presence (measured as flight initiation distance) during the COVID-19 shutdowns. We collected 6369 flight initiation distance estimates for 147 bird species and found that birds tolerated approaching humans to a similar level before and during the COVID-19 shutdowns. Moreover, during the shutdowns, bird escape behaviour did not consistently change with the level of governmental restrictions (measured as the stringency index). Hence, our results indicate that birds do not flexibly and quickly adjust their escape behaviour to the reduced human presence; in other words, the breeding populations of urban birds examined ...

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Diversity of incubation rhythms in a facultatively uniparental shorebird – the Northern Lapwing

Scientific Reports, Mar 18, 2019

Lapwing population, nest attendance highly correlates with actual incubation (warming or shading ... more Lapwing population, nest attendance highly correlates with actual incubation (warming or shading of eggs 13,24,32 ; Supplementary actograms 33). Also, females and males seem to heat the cutch to the similar temperatures (13,24,32,34 ; Supplementary actograms 33). We specifically investigated (1) between-nest variation in overall nest attendance (proportion of observed time parents were sitting on the nest or shading the eggs), (2) how male nest attendance relates to this between-nest variation in nest attendance, as a single parent cannot incubate with high nest attendance indefinitely, and (3) tested how incubation rhythm (female and male contribution) changed within a day, throughout the incubation period and season as food availability 35,36 , temperature and predation pressure 37,38 , as well as brood value vary over temporal time scales 39-41. Results overall nest attendance. Northern Lapwing parents incubated their eggs 87% of time (median, range: 68-94%, N = 60 nests with more than 2 days of recording; Fig. 1a, dark red and blue). Actual incubation bouts, defined as the time between the arrival of a parent at the nest and its departure, followed by the incubation of its partner (i.e. the total time allocated to a single parent including incubation recesses), covered 98% of observed time (median, range: 95-100%, N = 55 nests incubated by both parents; Fig. 1a, red and blue). In other words,

Sperm traits of the three genetic morphs in the ruff sandpiper

The ruff sandpiperCalidris pugnaxis a Palearctic lekking shorebird with three genetic morphs dete... more The ruff sandpiperCalidris pugnaxis a Palearctic lekking shorebird with three genetic morphs determined by an autosomal inversion. Male morphs differ strikingly in body size, ornaments, endocrinology and mating behavior. Aggressive Independents represent the ancestral haplotype, semi-cooperative Satellites and female-mimicking Faeders the inverted haplotypes. Since one inversion breakpoint is homozygous lethal, the inverted haplotypes (Satellite and Faeder) cannot recombine and are expected to accumulate mutations. The inversion regions also harbor genes involved in spermatogenesis. However, it is unknown whether the genetic difference between the morphs also translate into differences in sperm traits. Here, we use a captive-bred population of ruffs to compare sperm velocity and morphology among the morphs. Faeder sperm moved the slowest, which is in line with expectations from mutation accumulation and the idea that Faeders might fare worse than Satellites, as Satellite haplotype a...

Supporting information for 'Nest relief in the cryptically incubating semipalmated sandpiper is quick, but vocal

OSF, Sep 2, 2019

Supporting information for 'Diel timing of nest predation changes across breeding season in a subtropical shorebird

The data supporting the results, computer code used to generate the results, and the Supplementar... more

S5_Data_xlsx

Data for Fig 1B: Strength of assortative mating for size as a function of data source

S3_Data.xlsx

Unpublished data (nine long-term field studies): Data where we combined the information from data... more

Datasets

DATASET

Data from: Biparental incubation patterns in a high-Arctic breeding shorebird: how do pairs divide their duties?

In biparental species, parents may be in conflict over how much they invest into their offspring.... more In biparental species, parents may be in conflict over how much they invest into their offspring. To understand this conflict, parental care needs to be accurately measured, something rarely done. Here, we quantitatively describe the outcome of parental conflict in terms of quality, amount and timing of incubation throughout the 21 day incubation period in a population of semipalmated sandpipers (Calidris pusilla) breeding under continuous daylight in the High Arctic. Incubation quality, measured by egg temperature and incubation constancy, showed no marked difference between the sexes. The amount of incubation, measured as length of incubation bouts, was on average 51 min longer per bout for females (11.5 h) than for males (10.7 h), at first glance suggesting that females invested more than males. However, this difference may have been offset by sex-differences in the timing of incubation; females were more often off-nest during the warmer period of the day, when foraging conditions were presumably better. Overall, the daily timing of incubation shifted over the incubation period (e. g., for female incubation from ‘evening-night’ to ‘night-morning’) and over the season, but varied considerably among pairs. At one extreme, pairs shared the amount of incubation equally, but one parent always incubated during the colder part of the day; at the other extreme, pairs shifted the start of incubation bouts between days so that each parent experienced similar conditions across the incubation period. Our results highlight how the simultaneous consideration of different aspects of care across time allows sex-specific investment to be more accurately quantified