Biology subjects

Bulla, M.

Publications and source records attributed to Bulla, M..

12 recordsLinked to original sources

bioRxiv2026

Global patterns and evolution of avian song complexity

Why birds evolved complex songs has been a long-standing puzzle. Here, by quantifying song complexity in 4,940 species (83% of all passerines), we show a latitudinal gradient in song complexity, with the most complex songs occurring in temperate, open-habitat bird assemblages characterized by relatively inconspicuous plumage. Using comparative analyses controlled for common ancestry, we find little support for traditional explanations based on sexual selection intensity, intelligence signaling, or species richness. Instead, complex songs evolve primarily in song-learning passerines, especially migrants, habitat generalists, and species breeding in open habitats where structured acoustic signals transmit more efficiently. Together, our findings indicate that global variation in song complexity emerges from the interaction between vocal learning, ecological context, and evolutionary history rather than from a single selective driver.

evolutionary biology↗

bioRxiv2023

Sperm traits of the three genetic morphs in the ruff sandpiper

BackgroundThe 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, while female-mimicking Faeders and semi-cooperative Satellites are the inverted haplotypes. Because one inversion breakpoint is homozygous lethal, the inverted haplotypes cannot recombine and are expected to accumulate deleterious mutations. The inversion regions also harbor genes involved in spermatogenesis. However, it remains unknown whether the genetic differences between the morphs also translate into differences in sperm traits. Here, we use a captive-bred population of ruffs to compare sperm swimming speed and morphology among the morphs. ResultsRuff sperm morphologically resembled those of passerines, but moved differently, vibrating from side to side while slowly moving forward, rather than rotating while moving forward. Faeder sperm moved the slowest, which is consistent with the prediction of genetic deterioration over time. However, against expectation, sperm of Independents did not seem to be of the highest quality, i.e., their sperm were not the fastest nor the least variable, and they had sperm with 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 weakly positively correlated with head length (absolute and relative). ConclusionsThe three genetically determined ruff morphs showed subtle differences in swimming speed and in the length of some sperm components. However, the between-morph differences in sperm swimming speed were not linked to the differences in morphology. We conclude that there is at best limited evidence for lower-quality sperm in the morphs that carry the inversion, and suggest that the potential for the evolution of morph-specific sperm adaptations may be limited in this system. Lay SummaryThe ruff sandpiper is a shorebird that exhibits three genetically distinct types of males, which differ markedly in body size, ornaments, hormones, and mating behavior. Aggressive Independents represent the type that evolved first. Semi-cooperative Satellites and female-mimicking Faeders evolved later through a specific type of genetic rearrangement called an inversion, in which a segment of a chromosome reversed in orientation. Due to the nature of this inversion, Satellite and Faeder chromosomes are expected to deteriorate over time. However, it remains unclear whether the genetic differences between these morphs, which affect physiological and behavioral traits, also translate into differences in sperm traits. We used a captive population of ruffs to compare sperm swimming speed and length measurements between the three types of males. Faeder sperm was the slowest, which is consistent with expectations based on genetic deterioration over time. However, against our expectations, the sperm of Independents does not appear to have better performance characteristics. Although the midpiece of a sperm is responsible for energy production, the length of the midpiece did not relate to sperm swimming speed.

evolutionary biology↗

bioRxiv2022

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

The coronavirus disease 2019 (COVID-19) pandemic dramatically altered human activities, and, during shutdowns. Here, we evaluated whether urban birds from five countries changed their tolerance towards humans during the COVID-19 shutdowns. We collected 6369 flight initiation distance estimates for 147 bird species and found that human numbers in parks (at a given hour, day, week or year - before and during the COVID-19 shutdowns) had a little effect on birds tolerance of approaching humans. Apart from the actual human numbers in the area (hourly scale), the effect of human activity at other temporal scales centered around zero. The results were similar across countries, for most species or when we restricted our analyses only to species sampled both before and during the COVID-19 shutdowns. As expected, the level of daily human presence in parks (measured by Google Mobility Reports) correlated negatively with the stringency of governmental restrictions (a weekly proxy for human presence) and was overall lower during COVID-19 shutdowns than during the post-shutdown year (2022). Our results highlight the resilience of birds to changes in human numbers on multiple temporal scales, the complexities of linking animal fear responses to human behavior, and the challenge of quantifying both simultaneously in situ.

animal behavior and cognition↗

bioRxiv2021

Nest relief in the cryptically-incubating semipalmated sandpiper is quick but vocal

Biparental care requires coordination between parents. Such coordination might prove difficult if opportunities to communicate are scarce, which might have led to the evolution of elaborate and noisy nest relief rituals in species facing a low risk of predation. However, whether such conspicuous rituals also evolved in species that avoid predation by relying on crypsis remains unclear. Here, we used a continuous monitoring system to describe nest relief behavior during incubation in an Arctic-breeding shorebird with passive nest defense, the semipalmated sandpiper (Calidris pusilla). We then explored whether nest relief behavior provides information about parental cooperation and predicts incubation effort. We found that incubating parents vocalized twice as much before the arrival of their partner than during other times of incubation. In 75% of nest reliefs, the incubating parent left the nest only after its partner had returned and initiated the nest relief. In these cases, exchanges were quick (25s, median) and shortened over the incubation period by 0.1 - 1.4s per day (95%CI), suggesting that parents became more synchronized. However, nest reliefs were not cryptic. In 90% of exchanges, at least one parent vocalized, and in 20% of nest reliefs the incubating parent left the nest only after its returning partner called instantaneously. In 30% of cases, the returning parent initiated the nest relief with a call; in 39% of these cases, the incubating partner replied. If the partner replied, the next off-nest bout was 1 - 4hr (95%CI) longer than when the partner did not reply, which corresponds to an 8 - 45% increase. Our results indicate that incubating semipalmated sandpipers, which rely on crypsis to avoid nest predation, have quick but acoustically conspicuous nest reliefs. Our results also suggest that vocalizations during nest reliefs may be important for the division of parental duties. LAY SUMMARYO_LIBiparental care requires coordination between parents. In species where both parents incubate and nests are visible, parents often perform complex nest relief rituals. Is this also the case in species where nests are cryptic? C_LIO_LIWe video-recorded nest relief behavior at nests of cryptically incubating semipalmated sandpipers. C_LIO_LIParents relieved each other quickly, but they vocalized frequently. In 20% of nest reliefs the incubating parent left only after its returning partner called instantaneously. In 30% of cases the returning parent initiated the nest relief with a call. If the partner replied, its next off-nest bout was 1 - 4hr longer than when the partner did not reply, which corresponds to an 8 - 45% increase. C_LIO_LIOur results suggest that vocalizations during nest relief may be important for the division of parental duties. Further work in sandpipers and other taxa is needed to elucidate the role of parental vocalization in coordinating and synchronizing parental duties. C_LI

animal behavior and cognition↗

bioRxiv2021

Still no evidence for disruption of global patterns of nest predation in shorebirds

Many shorebird species are rapidly declining (Piersma et al. 2016; Munro 2017; Studds et al. 2017), but it is not always clear why. Deteriorating and disappearing habitat, e.g. due to intensive agriculture (Donal et al. 2001; Kentie et al. 2013; Kentie et al. 2018), river regulation (Nebel et al. 2008) or mudflat reclamation (Ma et al. 2014; Larson 2017), and hunting (Reed et al. 2018; Gallo-Cajiao et al. 2020) are some of the documented causes. A recent study suggests yet another possible cause of shorebird decline: a global increase in nest predation (Kubelka et al. 2018). The authors compiled an impressive dataset on patterns of nest predation in shorebirds and their analyses suggest that global patterns of nest predation have been disrupted by climate change, particularly in the Arctic. They go as far as to conclude that the Arctic might have become an ecological trap (Kubelka et al. 2018). Because these findings might have far-reaching consequences for conservation and related political decisions, we scrutinized the study and concluded that the main conclusions of Kubelka et al. (2018) are invalid (Bulla et al. 2019a). The authors then responded by reaffirming their conclusions (Kubelka et al. 2019b). Here, we evaluate some of Kubelka et al.s (2019b) responses, including their recent erratum (2020), and show that the main concerns about the original study still hold. Specifically, (1) we reaffirm that Kubelka et al.s (2018) original findings are confounded by study site. Hence, their conclusions are over-confident because of pseudo-replication. (2) We reiterate that there is no statistical support for the assertion that predation rate has changed in a different way in the Arctic compared to other regions. The relevant test is an interaction between a measure of time (year or period) and a measure of geography (e.g., Arctic vs the rest of the world). The effect of such an interaction is weak, uncertain and statistically non-significant, which undermines Kubelka et al.s (2018) key conclusion. (3) We further confirm that the suggested general increase in predation rates over time is at best a weak and uncertain trend. The most parsimonious hypothesis for the described results is that the temporal changes in predation rate are an artefact of temporal changes in methodology and data quality. Using only high-quality data, i.e. directly calculated predation rates, reveals no overall temporal trend in predation rate. Below we elaborate in detail on each of these points. We conclude that (i) there is no evidence whatsoever that the pattern in the Arctic is different from that in the rest of the world and (ii) there is no solid evidence for an increase in predation rate over time. While we commend Kubelka et al. for compiling and exploring the data, we posit that the data underlying their study, and perhaps all currently available data, are not sufficient (or of sufficient quality) to test their main hypotheses. We call for standardized and consistent data collection protocols and experimental validation of current methods for estimating nesting success.

ecology↗

bioRxiv2020

A global analysis of song frequency in passerines provides no support for the acoustic adaptation hypothesis but suggests a role for sexual selection

Many animals use acoustic signals for communication, implying that the properties of these signals can be under strong selection. The acoustic adaptation hypothesis predicts that species living in dense habitats emit lower-frequency sounds than those in open areas, because low-frequency sounds generally propagate further in denser vegetation. Signal frequency may also be under sexual selection, because it correlates with body size and lower-frequency sounds are perceived as more intimidating. Here, we evaluate these hypotheses by analysing variation in peak song frequency across 5,085 passerine species (Passeriformes). A phylogenetically-informed analysis revealed that song frequency decreases with increasing body mass and with male-biased sexual size dimorphism. However, we found no support for the predicted relationship between frequency and habitat. Our results suggest that the global variation in passerine song frequency is mostly driven by natural and sexual selection causing evolutionary shifts in body size rather than by habitat-related selection on sound propagation. Statement of authorshipTA and PM conceived and designed the study with input from all authors. TA and BK coordinated the study. PM collected the song data. MV performed the statistical analyses with input from WF. MB made the figures with help from MV and PM. TP and HB provided bioacoustic expertise. PM drafted the first version of the manuscript. TA, BK and PM revised and finalized the manuscript with input from all authors. Data availability statementThe data used in this study were collected from publicly available databases. All data and computer code used to generate the results, as well as supplementary figures and tables will be freely available at https://osf.io/fa9ky/.

evolutionary biology↗

bioRxiv2019

No evidence for disruption of global patterns of nest predation in shorebirds

Kubelka et al. (Science, 9 November 2018, p. 680-683) claim that climate change has disrupted patterns of nest predation in shorebirds. They report that predation rates have increased since the 1950s, especially in the Arctic. We describe methodological problems with their analyses and argue that there is no solid statistical support for their claims.

ecology↗

bioRxiv2018

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

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.

animal behavior and cognition↗

bioRxiv2017

Methods in field chronobiology

Chronobiological research has seen a continuous development of novel approaches and techniques to measure rhythmicity at different levels of biological organization from locomotor activity (e.g. migratory restlessness) to physiology (e.g. temperature and hormone rhythms, and relatively recently also in genes, proteins and metabolites). However, the methodological advancements in this field have been mostly and sometimes exclusively used only in indoor laboratory settings. In parallel, there has been an unprecedented and rapid improvement in our ability to track animals and their behaviour in the wild. However, while the spatial analysis of tracking data is widespread, its temporal aspect is largely unexplored. Here, we review the tools that are available or have potential to record rhythms in the wild animals with emphasis on currently overlooked approaches and monitoring systems. We then demonstrate, in three question-driven case studies, how the integration of traditional and newer approaches can help answer novel chronobiological questions in free-living animals. Finally, we highlight unresolved issues in field chronobiology that may benefit from technological development in the future. As most of the studies in the field are descriptive, the future challenge lies in applying the diverse technologies to experimental set-ups in the wild.

animal behavior and cognition↗

bioRxiv2017

Temporary mate removal during incubation leads to variable compensation in a biparental shorebir

Biparental care for offspring requires cooperation, but it is also a potential source of conflict, since one parent may care less at the expense of the other. How, then, do parents respond to the reduction of their partners care? Theoretical models predict that parents that feed offspring should partially compensate for the reduced care of their partner. However, for incubating birds partial compensation is unlikely the optimal strategy, because the entire brood can fail with reduced care. Although biparental incubation dominates in non-passerine birds, short-term manipulations of parental care and evaluations of individual differences in the response, both crucial to our understanding of parental cooperation, are scarce. Here, we describe the response of semipalmated sandpiper (Calidris pusilla) parents to a 24-hour removal of their partner during the incubation period, explore factors that can explain individual variation in the response, and describe how incubation rhythms changed after the removed parent returned. On average, the parents compensated partially for the absence of their partners care (59%; 95%CI: 49-70%, N = 25 individuals). The level of compensation did not differ between the sexes. However, individual responses varied from no to full compensation (2-101%). In seven nests where the removed parent never returned, the widowed parent attended the nest for 0-10 days (median: 4 days). In contrast to patterns observed in undisturbed nests or in uniparental species, nest attendance during compensation tended to be higher during the warmer part of the day. Although the level of compensation was not related to the before-experimental share of incubation, more responsive parents (that left the nest earlier upon human approach) compensated more. The quality of incubation in the after-experimental period was lower than usual, but improved quickly over time. Our findings suggest that full compensation might be limited by energetic constraints or by variation in responsiveness to the absence of the partner. Nevertheless, semipalmated sandpiper parents are able to adjust their subsequent incubation behaviour to take full responsibility for the nest when widowed. Because (nearly) full compensation was the most common response, we speculate that all individuals attempt full compensation, but that some fail because their energy stores get depleted, or because they are less responsive to the absence of their partner.

animal behavior and cognition↗

bioRxiv2017

Flexible Parental Care: Uniparental Incubation In Biparentally Incubating Shorebirds

Recent findings suggest that relative investment of females and males into parental care depends on the populations adult sex-ratio. For example, all else being equal, males should be the more caring sex if the sex ratio is male biased. Whether such outcomes are evolutionary fixed (i.e. related to the species typical sex-ratio) or whether they arise through flexible responses of individuals to the current population sex-ratio remains unclear. Nevertheless, a flexible response might be limited by evolutionary history when one sex loses the ability to care or when a single parent cannot successfully care. Here, we demonstrate that after the disappearance of one parent, individuals from 8 out of 15 biparentally incubating shorebird species were able to incubate uniparentally for 1-19 days (median = 3, N = 69). Such uniparental phases often resembled the incubation rhythm of species with obligatory uniparental incubation. Although it has been suggested that females of some shorebirds desert their brood after hatching, our findings indicate that either sex may desert prior to hatching. Strikingly, in 27% of uniparentally incubated clutches - from 5 species - we document successful hatching. Our data thus reveal the potential for a flexible switch from biparental to uniparental care.

evolutionary biology↗

bioRxiv2016

Unexpected diversity in socially synchronized rhythms of shorebirds

The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment1-4. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions1,5, but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators6-10. Individuals can temporally segregate their daily activities (e.g. prey avoiding predators, subordinates avoiding dominants) or synchronize their activities (e.g. group foraging, communal defence, pairs reproducing or caring for offspring)6-9,11. The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood5-7,9. Here, we address this in the context of biparental care, a particularly sensitive phase of social synchronization12 where pair members potentially compromise their individual rhythms. Using data from 729 nests of 91 populations of 32 biparentally-incubating shorebird species, where parents synchronize to achieve continuous coverage of developing eggs, we report remarkable within- and between-species diversity in incubation rhythms. Between species, the median length of one parents incubation bout varied from 1 - 19 hours, while period length-the time in which a parents probability to incubate cycles once between its highest and lowest value - varied from 6 - 43 hours. The length of incubation bouts was unrelated to variables reflecting energetic demands, but species relying on crypsis (the ability to avoid detection by other animals) had longer incubation bouts than those that are readily visible or actively protect their nest against predators. Rhythms entrainable to the 24-h light-dark cycle were less prevalent at high latitudes and absent in 18 species. Our results indicate that even under similar environmental conditions and despite 24-h environmental cues, social synchronization can generate far more diverse behavioural rhythms than expected from studies of individuals in captivity5-7,9. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms.

animal behavior and cognition↗