Breeding site fidelity is lower in polygamous shorebirds and male-biased in monogamous species.

Sex-bias in breeding dispersal is considered the norm in many taxa, and the magnitude and direction of such sex-bias is expected to correlate with the social mating system. We used local return rates in shorebirds as an index of breeding site fidelity, and hence as an estimate of the propensity for breeding dispersal, and tested whether variation in site fidelity and in sex-bias in site fidelity relates to the mating system. Among 111 populations of 49 species, annual return rates to a breeding site varied between 0% and 100%. After controlling for body size (linked to survival) and other confounding factors, monogamous species showed higher breeding site fidelity compared with polyandrous and polygynous species. Overall, there was a strong male bias in return rates, but the sex-bias in return rate was independent of the mating system and did not covary with the extent of sexual size dimorphism. Our results bolster earlier findings that the sex-biased dispersal is weakly linked to the mating system in birds. Instead, our results show that return rates are strongly correlated with the mating system in shorebirds regardless of sex. This suggests that breeding site fidelity may be linked to mate fidelity, which is only important in the monogamous, biparentally incubating species, or that the same drivers influence both the mating system and site fidelity. The strong connection between site fidelity and the mating system suggests that variation in site fidelity may have played a role in the coevolution of the mating system, parental care, and migration strategies.

Diel timing of nest predation changes across breeding season in a subtropical shorebird.

Predation is the most common cause of nest failure in birds. While nest predation is relatively well studied in general, our knowledge is unevenly distributed across the globe and taxa, with, for example, limited information on shorebirds breeding in subtropics. Importantly, we know fairly little about the timing of predation within a day. Here, we followed 444 nests of the red-wattled lapwing (Vanellus indicus), a ground-nesting shorebird, for a sum of 7,828 days to estimate a nest predation rate, and continuously monitored 230 of these nests for a sum of 2,779 days to reveal how the timing of predation changes over the day and season in a subtropical desert. We found that 312 nests (70%) hatched, 76 nests (17%) were predated, 23 (5%) failed for other reasons, and 33 (7%) had an unknown fate. Daily predation rate was 0.95% (95%CrI: 0.76% - 1.19%), which for a 30-day long incubation period translates into ~25% (20% - 30%) chance of nest being predated. Such a predation rate is low compared to most other avian species. Predation events (N = 25) were evenly distributed across day and night, with a tendency for increased predation around sunrise, and evenly distributed also across the season, although night predation was more common later in the season, perhaps because predators reduce their activity during daylight to avoid extreme heat. Indeed, nests were never predated when midday ground temperatures exceeded 45℃. Whether the diel activity pattern of resident predators undeniably changes across the breeding season and whether the described predation patterns hold for other populations, species, and geographical regions await future investigations.

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

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 in dense habitats emit lower-frequency sounds than those in open areas because low-frequency sounds propagate further in dense vegetation than high-frequency sounds. 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.

Comment on "Global pattern of nest predation is disrupted by climate change in shorebirds".

Kubelka et al (Reports, 9 November 2018, p. 680) 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.

Nest initiation and flooding in response to season and semi-lunar spring tides in a ground-nesting shorebird.

BACKGROUND: Marine and intertidal organisms face the rhythmic environmental changes induced by tides. The large amplitude of spring tides that occur around full and new moon may threaten nests of ground-nesting birds. These birds face a trade-off between ensuring nest safety from tidal flooding and nesting near the waterline to provide their newly hatched offspring with suitable foraging opportunities. The semi-lunar periodicity of spring tides may enable birds to schedule nest initiation adaptively, for example, by initiating nests around tidal peaks when the water line reaches the farthest into the intertidal habitat. We examined the impact of semi-lunar tidal changes on the phenology of nest flooding and nest initiation in Snowy Plovers (Charadrius nivosus) breeding at Bahía de Ceuta, a coastal wetland in Northwest Mexico. RESULTS: Using nest initiations and fates of 752 nests monitored over ten years we found that the laying season coincides with the lowest spring tides of the year and only 6% of all nests were flooded by tides. Tidal nest flooding varied substantially over time. First, flooding was the primary cause of nest failures in two of the ten seasons indicating high between-season stochasticity. Second, nests were flooded almost exclusively during the second half of the laying season. Third, nest flooding was associated with the semi-lunar spring tide cycle as nests initiated around spring tide had a lower risk of being flooded than nests initiated at other times. Following the spring tide rhythm, plovers appeared to adapt to this risk of flooding with nest initiation rates highest around spring tides and lowest around neap tides. CONCLUSIONS: Snowy Plovers appear generally well adapted to the risk of nest flooding by spring tides. Our results are in line with other studies showing that intertidal organisms have evolved adaptive responses to predictable rhythmic tidal changes but these adaptations do not prevent occasional catastrophic losses caused by stochastic events.

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

In birds, incubation by both parents is a 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 course of the day and breeding season, detailed descriptions of this variation are rare, especially in species with variable male contributions to care. Here, we continuously video-monitored 113 nests of Northern Lapwings Vanellus vanellus to reveal the diversity of incubation rhythms and parental involvement, as well as their daily and seasonal variation. We found great between-nest variation in the overall nest attendance (68-94%; median = 87%) and in how much males attended their nests (0-37%; median = 13%). Notably, the less the males attended their nests, the lower was the overall nest attendance, even though females partially compensated for the males' decrease. Also, despite seasonal environmental trends (e.g. increasing temperature), incubation rhythms changed little over the season and 27-day incubation period. However, as nights shortened with the progressing breeding season, the longest night incubation bout of females shortened too. Importantly, within the 24h-day, nest attendance was highest, incubation bouts longest, exchange gaps shortest and male involvement lowest during the night. Moreover, just after sunrise and before sunset males attended the nest the most. To conclude, we confirm substantial between nest differences in Lapwing male nest attendance, reveal how such differences relates to variation in incubation rhythms, and describe strong circadian incubation rhythms modulated by sunrise and sunset.

Scrutinizing assortative mating in birds.

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.

Flexible parental care: Uniparental incubation in biparentally incubating shorebirds.

The relative investment of females and males into parental care might depend on the population's 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 the evolutionary history of the species, because one sex may have lost the ability to care or because a single parent cannot successfully raise the brood. 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). Moreover, their daily incubation rhythm often resembled that of obligatory uniparental shorebird species. Although it has been suggested that in some biparental shorebirds females desert their brood after hatching, we found both sexes incubating uniparentally. Strikingly, in 27% of uniparentally incubated clutches - from 5 species - we documented successful hatching. Our data thus reveal the potential for a flexible switch from biparental to uniparental care.

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.This article is part of the themed issue 'Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals'.

Marine biorhythms: bridging chronobiology and ecology.

Marine organisms adapt to complex temporal environments that include daily, tidal, semi-lunar, lunar and seasonal cycles. However, our understanding of marine biological rhythms and their underlying molecular basis is mainly confined to a few model organisms in rather simplistic laboratory settings. Here, we use new empirical data and recent examples of marine biorhythms to highlight how field ecologists and laboratory chronobiologists can complement each other's efforts. First, with continuous tracking of intertidal shorebirds in the field, we reveal individual differences in tidal and circadian foraging rhythms. Second, we demonstrate that shorebird species that spend 8-10 months in tidal environments rarely maintain such tidal or circadian rhythms during breeding, likely because of other, more pertinent, temporally structured, local ecological pressures such as predation or social environment. Finally, we use examples of initial findings from invertebrates (arthropods and polychaete worms) that are being developed as model species to study the molecular bases of lunar-related rhythms. These examples indicate that canonical circadian clock genes (i.e. the homologous clock genes identified in many higher organisms) may not be involved in lunar/tidal phenotypes. Together, our results and the examples we describe emphasize that linking field and laboratory studies is likely to generate a better ecological appreciation of lunar-related rhythms in the wild.This article is part of the themed issue 'Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals'.

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 environment. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions, but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators. Individuals can temporally segregate their daily activities (for example, prey avoiding predators, subordinates avoiding dominants) or synchronize their activities (for example, group foraging, communal defence, pairs reproducing or caring for offspring). The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood. Here we investigate these rhythms in the context of biparental care, a particularly sensitive phase of social synchronization 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 parent's incubation bout varied from 1-19 h, whereas period length-the time in which a parent's probability to incubate cycles once between its highest and lowest value-varied from 6-43 h. 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 who 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 captivity. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms.

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

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 3.6min (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.

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. 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 51min longer per bout for females (11.5h) than for males (10.7h), 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.