Biological rhythms

Wild times

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Little is known about the biological rhythms that emerge from social behaviours in the wild. A study of shorebird pairs shows that rhythms of nest-incubation duties are mainly governed by strategies to avoid predators. See Letter p.109

Fundamental to all organisms, from bacteria to humans, is the daily oscillation of behaviour and physiology. During a 24-hour day, animals devote blocks of time to rest or activity1. The pace of the daily rhythm is mainly governed by an organism's circadian clock, which is synchronized to the daily light–dark cycle2,3,4,5. Biological rhythms can also be influenced by an organism's social environment; however, little is known about the factors that influence these social behavioural rhythms. On page 109, Bulla et al.6 report a large-scale study of the timing of daily nest-incubation duties shared between pairs of shorebirds.

Almost all studies of the daily rhythms of animals have used captive and individually housed laboratory strains under stringently controlled conditions. Such investigations have aided our understanding of biological rhythms; however, the survival of wild animals depends on their ability to shape their daily rhythms in response to complex external factors and, for many animals, on their ability to synchronize their activity with that of other individuals. Although rhythms of social behaviour are evident in nature2,5,7,8, there have been few investigations of the genetic and environmental factors that influence this phenomenon in wild animals.

Bulla and colleagues investigated a compelling natural model of social synchronization: the timing of shifts in nest attendance during egg incubation by individual pairs of shorebirds. Shorebird eggs require continuous incubation, and parents must precisely coordinate and synchronize their care of the nest. The authors report a 20-year study of incubation patterns of wild shorebirds, assembling a data set that includes 32 species, 729 pairs of birds and 91 populations that spanned high to low latitudes worldwide. They assessed incubation patterns using a combination of direct and indirect observation methods.

The authors found that the timing of individual incubation bouts ranged from just over 1 hour to an enormous 50 hours. The authors also calculated the durations of incubation periods, which reflect the average length of one cycle of shared parental incubation. Bulla et al. observed a diversity of incubation periods for the parental nest exchanges. Some pairs of birds synchronized their incubation periods around a 24-hour rhythm, whereas other pairs had incubation periods that were less than 20 hours or more than 28 hours. The authors also observed pairs of birds that exhibited free-running rhythms: near 24-hour rhythms that were not synchronized to the light–dark cycle. It is well established that most animals exhibit behavioural rhythms that are synchronized by the daily light–dark cycle, and these rhythms are known to be influenced by both genetic and environmental factors. Thus, the authors' observation of exceptional diversity in incubation rhythms, independent of habitat, both within the same species and across different shorebird species, was highly unexpected.

What factors might be responsible for the large diversity in incubation rhythms of wild shorebirds? Using sophisticated modelling approaches, the authors evaluated the contribution that genetics might make to this variability. Their results indicate that closely related bird species show similar incubation-rhythm patterns — a result consistent with other observations9,10,11 that biological rhythms are genetically heritable.

The authors investigated what other factors might shape incubation patterns. Nest incubation and food foraging are mutually exclusive behaviours, and it is reasonable to assume that incubation-bout length would be affected by a bird's energetic status. Small birds store less energy than large ones, use energy faster and should therefore need to forage more frequently. Thus, one might predict that bird species with a smaller body would exhibit more-frequent nest exchanges than larger species. However, Bulla et al. found no relationship between the body size of birds and the length of their incubation bouts.

Body-temperature regulation can also influence a bird's energetic demands. Birds in high-latitude, colder climates would be expected to deplete their energy stores more rapidly and show more-frequent incubation exchanges than birds in lower, warmer latitudes. However, Bulla and colleagues found that shorebirds in cold climates had longer bouts of incubation than birds in warmer climates. Together, these results indicate that incubation-bout length is not driven by a bird's energetic status.

Bulla et al. identified one behavioural factor that significantly influenced the duration of incubation bouts: the strategy used by parents to reduce predator attacks on the nest. Shorebirds nest on the ground, and use either parental camouflage or direct, attacking or distracting strategies to deter predators from attacking their nests. The birds that avoid predation through camouflage have long incubation bouts. This approach lessens the parental changeover activity that could reveal a nest location to predators. By contrast, shorebirds that actively respond to intruding predators to dissuade them from approaching have short incubation bouts (Fig. 1).

Figure 1: Nesting wild shorebirds use different strategies to avoid predators.
figure1

Gerrit Vyn/Nature Picture Library; Mike Wilkes/Nature Picture Library

Bulla et al.6 report a large-scale global study of nest-incubation timing patterns in pairs of wild shorebirds. a, The red knot (Calidris canutus rogersi) is camouflaged against its nesting background. The authors observed that this species exhibits long incubation bouts. This might help to avoid predation by reducing activity that could draw attention to the nest. b, The oystercatcher (Haematopus ostralegus) is not camouflaged against its nesting background, and instead actively responds to approaching predators. Bulla and colleagues noted that this species has short incubation bouts.

The diversity observed in incubation rhythms of pairs of shorebirds, both within the same species and across different species, is impressive, but perhaps Bulla and colleagues' most striking finding is their observation that only 22% of the parental pairs adopted a 24-hour pattern for their incubation rhythms. This finding is intriguing, because synchrony with the environment is considered an advantageous characteristic12, and such environmental asynchrony in animals is thought to have negative consequences, including associations with pathologies and early death13,14,15. Humans with disrupted biological rhythms can develop symptoms that range from those seen in relatively benign jet lag, to those of more serious conditions, such as obesity16, Alzheimer's disease17 and cancer18.

The work by Bulla and colleagues reveals diversity, flexibility and plasticity in the timing of a social behaviour, and challenges the assumption that animals maintain synchrony with the 24-hour day–night cycle. Does being out of synchrony with the environment exact a physiological cost on shorebirds, and if so, is the cost equally distributed in a given pair of birds? The incubation rhythm will probably favour one parent over the other because of differences in the natural phasing of food availability, predation risk and temperature for the parent away from the nest.

The finding that shorebird pairs of the same species can have substantially different incubation rhythms begs the question of how the rhythm is decided by a pair of birds. Is it a 'negotiation', or is the rhythm driven by the dominant partner? Is there year-to-year variation in the incubation rhythm for a given pair, and if so, what effect might fluctuating predator density have on the birds' rhythm? These and many other intriguing questions remain to be answered.Footnote 1

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Correspondence to C. Loren Buck.

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Buck, C. Wild times. Nature 540, 49–50 (2016). https://doi.org/10.1038/nature20481

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