Biological timekeeping in polar environments: lessons from terrestrial vertebrates.

The polar regions receive less solar energy than anywhere else on Earth, with the greatest year-round variation in daily light exposure; this produces highly seasonal environments, with short summers and long, cold winters. Polar environments are also characterised by a reduced daily amplitude of solar illumination. This is obvious around the solstices, when the Sun remains continuously above (polar 'day') or below (polar 'night') the horizon. Even at the solstices, however, light levels and spectral composition vary on a diel basis. These features raise interesting questions about polar biological timekeeping from the perspectives of function and causal mechanism. Functionally, to what extent are evolutionary drivers for circadian timekeeping maintained in polar environments, and how does this depend on physiology and life history? Mechanistically, how does polar solar illumination affect core daily or seasonal timekeeping and light entrainment? In birds and mammals, answers to these questions diverge widely between species, depending on physiology and bioenergetic constraints. In the high Arctic, photic cues can maintain circadian synchrony in some species, even in the polar summer. Under these conditions, timer systems may be refined to exploit polar cues. In other instances, temporal organisation may cease to be dominated by the circadian clock. Although the drive for seasonal synchronisation is strong in polar species, reliance on innate long-term (circannual) timer mechanisms varies. This variation reflects differing year-round access to photic cues. Polar chronobiology is a productive area for exploring the adaptive evolution of daily and seasonal timekeeping, with many outstanding areas for further investigation.

Genotypes selected for early and late avian lay date differ in their phenotype, but not fitness, in the wild.

Global warming has shifted phenological traits in many species, but whether species are able to track further increasing temperatures depends on the fitness consequences of additional shifts in phenological traits. To test this, we measured phenology and fitness of great tits (Parus major) with genotypes for extremely early and late egg lay dates, obtained from a genomic selection experiment. Females with early genotypes advanced lay dates relative to females with late genotypes, but not relative to nonselected females. Females with early and late genotypes did not differ in the number of fledglings produced, in line with the weak effect of lay date on the number of fledglings produced by nonselected females in the years of the experiment. Our study is the first application of genomic selection in the wild and led to an asymmetric phenotypic response that indicates the presence of constraints toward early, but not late, lay dates.

Ingrained city rhythms: flexible activity timing but more persistent circadian pace in urban birds.

Urbanization dramatically increases the amount of light at night, which may disrupt avian circadian organization. We measured activity patterns of great tits breeding in the city and forest, and subsequently measured two clock properties of these birds under controlled conditions: tau (endogenous circadian clock speed) and after-effects (history dependency of the clock relative to previous conditions). City and forest birds showed a high repeatability of activity onset (0.60 and 0.41, respectively), with no difference between habitats after controlling for date effects. Activity duration and offset showed more variance, without a difference between birds from the two habitats. Tau did not differ between city and forest birds, however, city birds showed stronger after-effects, taking more days to revert to their endogenous circadian period. Finally, onset of activity was correlated with clocks speed in both habitats. Our results suggest that potential differences in activity timing of city birds is not caused by different clock speeds, but by a direct response to light. Persistence in after-effects suggests a reduced sensitivity of the clock to light at night. Urbanization may select for clock properties that increase the inertia of the endogenous circadian system to improve accuracy of activity rhythms when exposed to noisier lighting cues.

Extreme bill dimorphism leads to different but overlapping isotopic niches and similar trophic positions in sexes of the charismatic extinct huia.

The New Zealand huia (Heteralocha acutirostris) had the most extreme bill sexual dimorphism among modern birds. Given the quick extinction of the species, the cause of the dimorphism could only be hypothesised to reflect different trophic niches and reduce male/female competition. We tested that hypothesis by combining museum specimens, geometric morphometrics, and isotopic analyses. We used geometric morphometrics to describe bill shape; measured bulk (δ15Nbulk) and (δ13Cbulk) values from feather as proxies of the birds' foraging habitat and diet; and compared compound-specific stable isotopes analyses (CSIA) of nitrogen in amino acids (δ15NAA) in male-female pairs to estimate their trophic position. Sexes had significantly different, but overlapping feather δ15Nbulk and δ13Cbulk values, but δ15NAA indicated identical trophic positions and δ15Nbulk was not related to bill shape. Trophic position was less variable among females, consistent with a specialised foraging behaviour and, thus, supporting a partial male/female foraging segregation.

Great tits do not compensate over time for a radio-tag-induced reduction in escape-flight performance.

The use of biologging and tracking devices is widespread in avian behavioral and ecological studies. Carrying these devices rarely has major behavioral or fitness effects in the wild, yet it may still impact animals in more subtle ways, such as during high power demanding escape maneuvers. Here, we tested whether or not great tits (Parus major) carrying a backpack radio-tag changed their body mass or flight behavior over time to compensate for the detrimental effect of carrying a tag. We tested 18 great tits, randomly assigned to a control (untagged) or one of two different types of a radio-tag as used in previous studies in the wild (0.9 g or 1.2 g; ~5% or ~6-7% of body mass, respectively), and determined their upward escape-flight performance 1, 7, 14, and 28 days after tagging. In between experiments, birds were housed in large free-flight aviaries. For each escape-flight, we used high-speed 3D videography to determine flight paths, escape-flight speed, wingbeat frequency, and actuator disk loading (ratio between the bird weight and aerodynamic thrust production capacity). Tagged birds flew upward with lower escape-flight speeds, caused by an increased actuator disk loading. During the 28-day period, all groups slightly increased their body mass and their in-flight wingbeat frequency. In addition, during this period, all groups of birds increased their escape-flight speed, but tagged birds did so at a lower rate than untagged birds. This suggests that birds may increase their escape-flight performance through skill learning; however, tagged birds still remained slower than controls. Our findings suggest that tagging a songbird can have a prolonged effect on the performance of rapid flight maneuvers. Given the absence of tag effects on reproduction and survival in most songbird radio-tagging studies, tagged birds in the wild might adjust their risk-taking behavior to avoid performing rapid flight maneuvers.

Polygenic basis for adaptive morphological variation in a threatened Aotearoa | New Zealand bird, the hihi (Notiomystis cincta).

To predict if a threatened species can adapt to changing selective pressures, it is crucial to understand the genetic basis of adaptive traits, especially in species historically affected by severe bottlenecks. We estimated the heritability of three hihi (Notiomystis cincta) morphological traits known to be under selection (nestling tarsus length, body mass and head-bill length) using 523 individuals and 39 699 single nucleotide polymorphisms (SNPs) from a 50 K Affymetrix SNP chip. We then examined the genetic architecture of the traits via chromosome partitioning analyses and genome-wide association scans (GWAS). Heritabilities estimated using pedigree relatedness or genomic relatedness were low. For tarsus length, the proportion of genetic variance explained by each chromosome was positively correlated with its size, and more than one chromosome explained significant variation for body mass and head-bill length. Finally, GWAS analyses suggested many loci of small effect contributing to trait variation for all three traits, although one locus (an SNP within an intron of the transcription factor HEY2) was tentatively associated with tarsus length. Our findings suggest a polygenic nature for the morphological traits, with many small effect size loci contributing to the majority of the variation, similar to results from many other wild populations. However, the small effective population size, polygenic architecture and already low heritabilities suggest that both the total response and rate of response to selection are likely to be limited in hihi.

Temperature has a causal and plastic effect on timing of breeding in a small songbird.

Phenotypic plasticity is an important mechanism by which an individual can adapt its seasonal timing to predictable, short-term environmental changes by using predictive cues. Identification of these cues is crucial to forecast the response of species to long-term environmental change and to study their potential to adapt. Individual great tits (Parus major) start reproduction early under warmer conditions in the wild, but whether this effect is causal is not well known. We housed 36 pairs of great tits in climate-controlled aviaries and 40 pairs in outdoor aviaries, where they bred under artificial contrasting temperature treatments or in semi-natural conditions, respectively, for two consecutive years, using birds from lines selected for early and late egg laying. We thus obtained laying dates in two different thermal environments for each female. Females bred earlier under warmer conditions in climate-controlled aviaries, but not in outdoor aviaries. The latter was inconsistent with laying dates from our wild population. Further, early selection line females initiated egg laying consistently ∼9 days earlier than late selection line females in outdoor aviaries, but we found no difference in the degree of plasticity (i.e. the sensitivity to temperature) in laying date between selection lines. Because we found that temperature causally affects laying date, climate change will lead to earlier laying. This advancement is, however, unlikely to be sufficient, thereby leading to selection for earlier laying. Our results suggest that natural selection may lead to a change in mean phenotype, but not to a change in the sensitivity of laying dates to temperature.

Timing manipulations reveal the lack of a causal link across timing of annual-cycle stages in a long-distance migrant.

Organisms need to time their annual-cycle stages, like breeding and migration, to occur at the right time of the year. Climate change has shifted the timing of annual-cycle stages at different rates, thereby tightening or lifting time constraints of these annual-cycle stages, a rarely studied consequence of climate change. The degree to which these constraints are affected by climate change depends on whether consecutive stages are causally linked (scenario I) or whether the timing of each stage is independent of other stages (scenario II). Under scenario I, a change in timing in one stage has knock-on timing effects on subsequent stages, whereas under scenario II, a shift in the timing of one stage affects the degree of overlap with previous and subsequent stages. To test this, we combined field manipulations, captivity measurements and geolocation data. We advanced and delayed hatching dates in pied flycatchers (Ficedula hypoleuca) and measured how the timing of subsequent stages (male moult and migration) were affected. There was no causal effect of manipulated hatching dates on the onset of moult and departure to Africa. Thus, advancing hatching dates reduced the male moult-breeding overlap with no effect on the moult-migration interval. Interestingly, the wintering location of delayed males was more westwards, suggesting that delaying the termination of breeding carries over to winter location. Because we found no causal linkage of the timing of annual-cycle stages, climate change could shift these stages at different rates, with the risk that the time available for some becomes so short that this will have major fitness consequences.

Short-term, but not long-term, increased daytime workload leads to decreased night-time energetics in a free-living song bird.

Reproduction is energetically expensive and to obtain sufficient energy, animals can either alter their metabolic system over time to increase energy intake (increased-intake hypothesis) or reallocate energy from maintenance processes (compensation hypothesis). The first hypothesis predicts a positive relationship between basal metabolic rate (BMR) and energy expenditure (DEE) because of the higher energy demands of the metabolic system at rest. The second hypothesis predicts a trade-off between different body functions, with a reduction of the BMR as a way to compensate for increased daytime energetic expenditure. We experimentally manipulated the workload of wild pied flycatchers by adding or removing chicks when chicks were 2 and 11 days old. We then measured the feeding frequency (FF), DEE and BMR at day 11, allowing us to assess both short- and long-term effects of increased workload. The manipulation at day 2 caused an increase in FF when broods were enlarged, but no response in DEE or BMR, while the manipulation at day 11 caused an increase in FF, no change in DEE and a decrease in BMR in birds with more chicks. Our results suggest that pied flycatchers adjust their workload but that this does not lead to a higher BMR at night (no support for the increased-intake hypothesis). In the short term, we found that birds reallocate energy with a consequent reduction of BMR (evidence for the compensation hypothesis). Birds thus resort to short-term strategies to increase energy expenditure, which could explain why energy expenditure and hard work are not always correlated in birds.

A songbird compensates for wing molt during escape flights by reducing the molt gap and increasing angle of attack.

During molt, birds replace their feathers to retain feather quality and maintain flight performance. However, wing gaps inherent of this process can also reduce flight capacities, which could be detrimental when foraging or escaping predators. Still, many bird species will not cease their normal activities when molting. In this study, we investigated whether and how birds adjust their escape flight behavior to compensate for the reduction in performance when flying with wing gaps. Using stereoscopic high-speed videography, we filmed 146 upward-directed escape flights of 19 and 22 pied flycatchers (Ficedula hypoleuca) with and without simulated molt gaps, respectively. We then reconstructed the three-dimensional body and wing movements throughout each maneuver. By comparing flights with and without gaps, we determined how wing molt gaps affected wing morphology and escape flight performance, and how the birds adjusted their flight kinematics in order to negate possible negative aerodynamic effects. Our manipulations resulted in a lower second moment of area of the wings, but flight speed and net aerodynamic force production did not differ between the two groups. We found that in manipulated birds, the size of the gap was reduced as the flight feathers adjacent to the gap had moved towards each other. Moreover, the experimental decrease in second moment of area was associated with an increase in angle of attack, whereas changes in wingbeat-induced speeds were associated with variations in aerodynamic force production. This suggests that the control of escape flight in molting birds might be modular, allowing relatively simple flight control, thus reducing the burden on the neuro-muscular flight control system.

Climate change leads to differential shifts in the timing of annual cycle stages in a migratory bird.

Shifts in reproductive phenology due to climate change have been well documented in many species but how, within the same species, other annual cycle stages (e.g. moult, migration) shift relative to the timing of breeding has rarely been studied. When stages shift at different rates, the interval between stages may change resulting in overlaps, and as each stage is energetically demanding, these overlaps may have negative fitness consequences. We used long-term data of a population of European pied flycatchers (Ficedula hypoleuca) to investigate phenological shifts in three annual cycle stages: spring migration (arrival dates), breeding (egg-laying and hatching dates) and the onset of postbreeding moult. We found different advancements in the timing of breeding compared with moult (moult advances faster) and no advancement in arrival dates. To understand these differential shifts, we explored which temperatures best explain the year-to-year variation in the timing of these stages, and show that they respond differently to temperature increases in the Netherlands, causing the intervals between arrival and breeding and between breeding and moult to decrease. Next, we tested the fitness consequences of these shortened intervals. We found no effect on clutch size, but the probability of a fledged chick to recruit increased with a shorter arrival-breeding interval (earlier breeding). Finally, mark-recapture analyses did not detect an effect of shortened intervals on adult survival. Our results suggest that the advancement of breeding allows more time for fledgling development, increasing their probability to recruit. This may incur costs to other parts of the annual cycle, but, despite the shorter intervals, there was no effect on adult survival. Our results show that to fully understand the consequences of climate change, it is necessary to look carefully at different annual cycle stages, especially for organisms with complex cycles, such as migratory birds.

Climate change relaxes the time constraints for late-born offspring in a long-distance migrant.

Animals in seasonal environments need to fit their annual-cycle stages, such as moult and migration, in a tight schedule. Climate change affects the phenology of organisms and causes advancements in timing of these annual-cycle stages but not necessarily at the same rates. For migratory birds, this can lead to more severe or more relaxed time constraints in the time from fledging to migration, depending on the relative shifts of the different stages. We tested how a shift in hatch date, which has advanced due to climate change, impacts the organization of the birds' whole annual cycle. We experimentally advanced and delayed the hatch date of pied flycatcher chicks in the field and then measured the timing of their annual-cycle stages in a controlled laboratory environment. Hatch date affected the timing of moult and pre-migratory fattening, but not migration. Early-born birds hence had a longer time to fatten up than late-born ones; the latter reduced their interval between onset of fattening and migration to be able to migrate at the same time as the early-born birds. This difference in time constraints for early- and late-born individuals may explain why early-born offspring have a higher probability to recruit as a breeding bird. Climate change-associated advancements of avian egg-lay dates, which in turn advances hatch dates, can thus reduce the negative fitness consequences of reproducing late, thereby reducing the selection for early egg-laying migratory birds.

The Kraken: when myth encounters science.

Hundreds of years ago, sailors were terrified by the Kraken, a dreadful sea monster capable of sinking ships and with a taste for human flesh. Today we know the legends of this monster were based on sightings of giant squids. This animal belongs to the genus Architeuthis and was the subject of many scientific studies. Despite its enormous size (up to 18m), the giant squid is astoundingly elusive and much of its biology remains unknown. Thus shrouded in mystery, Architeuthis is almost a mythological creature and has a place both in science and in myth: the very last of the legends to persist to this day.

The Kraken: when myth encounters science / O Kraken: quando mito e ciência se encontram

Hundreds of years ago, sailors were terrified by the Kraken, a dreadful sea monster capable of sinking ships and with a taste for human flesh. Today we know the legends of this monster were based on sightings of giant squids. This animal belongs to the genus Architeuthis and was the subject of many scientific studies. Despite its enormous size (up to 18m), the giant squid is astoundingly elusive and much of its biology remains unknown. Thus shrouded in mystery, Architeuthis is almost a mythological creature and has a place both in science and in myth: the very last of the legends to persist to this day.

Séculos atrás, marinheiros se amedrontavam com histórias do Kraken, um terrível monstro marinho capaz de afundar embarcações e devorar suas tripulações. Atualmente, sabemos que a lenda desse monstro foi baseada em encontros com lulas-gigantes. Esse animal pertence ao gênero Architeuthis e foi alvo de muitos estudos científicos. Apesar de seu enorme tamanho (pode chegar a 18m), a lula-gigante é incrivelmente elusiva e muito de sua biologia permanece desconhecida. Assim, envolto em mistério, Architeuthis é quase um ser mitológico, ocupando um lugar tanto na ciência como no mito: a última das lendas a persistir nos dias de hoje.

Modeling natural photic entrainment in a subterranean rodent (Ctenomys aff. knighti), the Tuco-Tuco.

Subterranean rodents spend most of the day inside underground tunnels, where there is little daily change in environmental variables. Our observations of tuco-tucos (Ctenomys aff. knighti) in a field enclosure indicated that these animals perceive the aboveground light-dark cycle by several bouts of light-exposure at irregular times during the light hours of the day. To assess whether such light-dark pattern acts as an entraining agent of the circadian clock, we first constructed in laboratory the Phase Response Curve for 1 h light-pulses (1000lux). Its shape is qualitatively similar to other curves reported in the literature and to our knowledge it is the first Phase Response Curve of a subterranean rodent. Computer simulations were performed with a non-linear limit-cycle oscillator subjected to a simple model of the light regimen experienced by tuco-tucos. Results showed that synchronization is achieved even by a simple regimen of a single daily light pulse scattered uniformly along the light hours of the day. Natural entrainment studies benefit from integrated laboratory, field and computational approaches.

Field and laboratory studies provide insights into the meaning of day-time activity in a subterranean rodent (Ctenomys aff. knighti), the tuco-tuco.

South American subterranean rodents (Ctenomys aff. knighti), commonly known as tuco-tucos, display nocturnal, wheel-running behavior under light-dark (LD) conditions, and free-running periods >24 h in constant darkness (DD). However, several reports in the field suggested that a substantial amount of activity occurs during daylight hours, leading us to question whether circadian entrainment in the laboratory accurately reflects behavior in natural conditions. We compared circadian patterns of locomotor activity in DD of animals previously entrained to full laboratory LD cycles (LD12:12) with those of animals that were trapped directly from the field. In both cases, activity onsets in DD immediately reflected the previous dark onset or sundown. Furthermore, freerunning periods upon release into DD were close to 24 h indicating aftereffects of prior entrainment, similarly in both conditions. No difference was detected in the phase of activity measured with and without access to a running wheel. However, when individuals were observed continuously during daylight hours in a semi-natural enclosure, they emerged above-ground on a daily basis. These day-time activities consisted of foraging and burrow maintenance, suggesting that the designation of this species as nocturnal might be inaccurate in the field. Our study of a solitary subterranean species suggests that the circadian clock is entrained similarly under field and laboratory conditions and that day-time activity expressed only in the field is required for foraging and may not be time-dictated by the circadian pacemaker.