Martin Bulla

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

Lay summary: Parents may be in conflict over the care they provide to their offspring. To understand this conflict, an accurate description of who does what and when is necessary. We used an automated system to continuously monitor which parent incubated the eggs in an arctic breeding shorebird. Birds sat on the eggs around 11 h at a time, but females sat longer than males. In compensation, females were off-duty more when feeding was easier.

EGGSHELL SPOTTING DOES NOT PREDICT MALE INCUBATION BUT MARKS THINNER AREAS OF A SHOREBIRD'S SHELLS

ABSTRACT. Many birds lay eggs speckled with black or reddish-brown spots of protoporphyrin pigment, but the function of these spots is debated. Two recent hypotheses have received considerable attention. Under the “signaling-function hypothesis,” speckling reflects female quality and influences allocation of male parental care; under the “structural-function hypothesis,” the speckles strengthen the eggshell when calcium is scarce. The evidence for each is taxonomically uneven. For instance, evidence for the signaling-function hypothesis comes from cavity-nesting and uniparentally incubating species in which the viewing conditions and possibilities for males to assess the speckling are limited, and male response to speckling is indirect (i.e., female-feeding) or postponed (i.e., chickfeeding). We tested the predictions of both hypotheses in a biparentally incubating ground-nesting shorebird, the Northern Lapwing (Vanellus vanellus), in which the potential for a direct male response to eggshell speckling exists and visual inspection of the eggs is not hindered by light availability in a nest cavity. The speckling parameters (spot intensity, distribution, and cover) were repeatable within Northern Lapwing clutches, a requirement for a sexually selected signal, but we found no relationship between male incubation and speckling. However, the spots were associated with thinner areas of eggshell, which strongly supports the suggestion of a structural (strengthening) function. Our results do not support the signaling-function hypothesis of eggshell speckling, but extend the structural-function hypothesis and prior findings (that speckling occurs primarily at thinner areas of the shell) to other avian taxa. Furthermore, if the generally accepted view that Northern Lapwing eggs are cryptically marked is correct, our findings suggest that more than one significant function can drive the evolution of avian eggshell pigmentation.

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’.

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.

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 others 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’.

Unusual incubation: Long-billed Dowitcher incubates mammalian bones

It is well established that once birds have laid their eggs they sometimes incubate non-egg objects. However, reports of birds incubating solely non-egg objects (without prior manipulation by researchers) are rare. Here we report on our observation of a Long-billed Dowitcher Limnodromus scolopaceus incubating a clutch composed entirely of mammalian bones. To our knowledge, this is the first report on (a) incubation of foreign objects in Scolopacidae, (b) incubation of a ‘clutch’ composed entirely of bones, and (c) incubation of foreign objects in a nest atypical for this species in both construction and nest habitat. We discuss possible explanations for this presumably maladaptive behaviour.

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

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 partner’s 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 partner’s 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.