Barbara M. Tomotani

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.

Timing avian long-distance migration: from internal clock mechanisms to global flights

Migratory birds regularly perform impressive long-distance flights, which are timed relative to the anticipated environmental resources at destination areas that can be several thousand kilometres away. Timely migration requires diverse strategies and adaptations that involve an intricate interplay between internal clock mechanisms and environmental conditions across the annual cycle. Here we review what challenges birds face during long migrations to keep track of time as they exploit geographically distant resources that may vary in availability and predictability, and summarize the clock mechanisms that enable them to succeed. We examine the following challenges: departing in time for spring and autumn migration, in anticipation of future environmental conditions; using clocks on the move, for example for orientation, navigation and stopover; strategies of adhering to, or adjusting, the time programme while fitting their activities into an annual cycle; and keeping pace with a world of rapidly changing environments. We then elaborate these themes by case studies representing long-distance migrating birds with different annual movement patterns and associated adaptations of their circannual programmes. We discuss the current knowledge on how endogenous migration programmes interact with external information across the annual cycle, how components of annual cycle programmes encode topography and range expansions, and how fitness may be affected when mismatches between timing and environmental conditions occur. Lastly, we outline open questions and propose future research directions. This article is part of the themed issue ‘Wild clocks: integrating chronobiology and ecology to understand timekeeping in free-living animals’.

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.

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.

Simulated moult reduces flight performance but overlap with breeding does not affect breeding success in a long‐distance migrant

1. Long-distance migrants are time-constrained as they need to incorporate many annual cycle stages within a year. Migratory passerines moult in the short interval between breeding and migration. To widen this interval, moult may start while still breeding, but this results in flying with moulting wings when food provisioning. 2. We experimentally simulated wing gaps in breeding male pied flycatchers by plucking 2 primary feathers from both wings. We quantified the nest visitations of both parents, proportion of high-quality food brought to the nestlings and adults and nestlings condition. Differences in oxidative damage caused by a possible reduction in flight efficiency were measured in amounts of ROMs and OXY in the blood. We also measured how flight performance was affected with recordings of the males escape flight using high-speed cameras. Finally, we collected data on adult survival, clutch size and laying date in the following year. 3. “Plucked” males travelled a 5% shorter distance per wingbeat, showing that our treatment reduced flight performance. In line with this, “plucked” males visited their nests less often. Females of “plucked” males, however, visited the nest more often than controls, and fully compensated their partners reduced visitation rate. As a result, there were no differences between treatments in food quality brought to the nest, adult or chick mass or number of successfully fledged chicks. Males did not differ in their oxidative damage or local survival to the following year. In contrast, females paired with plucked males tended to return less often to breed in the next year in comparison to controls, but this difference was not significant. For the birds that did return there were no effects on breeding. 5. Our results reveal that wing gaps in male pied flycatchers reduce their flight performance, but when it occurs during breeding they prioritise their future reproduction by reducing parental care. As a result, there is no apparent detriment to their condition during breeding. Because non-moulting females are able to compensate their partners reduced care, there is also no immediate costs to the offspring, but females may pay the cost suffering from a reduced survival. This article is protected by copyright. All rights reserved.

Social modulation of the daily activity rhythm in a solitary subterranean rodent, the tuco-tuco (Ctenomys sp).

South American subterranean rodents are mainly described as solitary and mutual synchronization was never observed among individuals maintained together in laboratory. We report that a single birth event was capable of disrupting the robust nocturnal activity rhythm of singly housed tuco-tucos from north-west Argentina. “Around-the-clock activity” was displayed by 8 out of 13 animals whose cages were closer to the newborn pups. However, experimental exposure to a pup vocalization did not produce a similar effect on the rhythms of adult animals. Our results indicate an effect of social interaction in the expression of biological rhythms even in solitary animals.

Diurnos ou Noturnos? Discutindo padrões temporais de atividade

Resumo. A classificacao de um animal como diurno ou noturno parece, a primeira vista, extremamente simples quando se caracteriza o comportamento geral. Entretanto, tal distincao nao e tao evidente nem na natureza e nem nas condicoes artificiais de laboratorio. Atualmente, os mecanismos fisiologicos que definem mamiferos diurnos e noturnos estao sendo investigados em diversos niveis biologicos. Relatos de animais com fases diferentes de atividade em laboratorio e em campo estao aumentando, podendo revelar um aspecto fundamental da organizacao temporal, especialmente em mamiferos. Palavras-chave. Arrastamento, mascaramento, ritmo diario, roedores.

Climate Change Impacts: Birds

Climate change can affect populations and species in various ways. Rising temperatures can shift geographical distributions and lead to (phenotypic or genetic) changes in traits, mostly phenology, which may affect demography. Most of these effects are well documented in birds. For example, the distribution of species has shifted polewards, and birds are nowadays breeding or migrating earlier. An important aspect of the observed phenological changes is whether species are thereby able to maintain synchrony with phenological changes in their environment, for example the phenology of their prey species. Disrupted synchrony, for example between predator and prey, can lead to reduced reproductive success or survival, which can negatively affect demography. Evidence for this happening in birds is – so far – limited but theoretical models predict that extinction risks could arise through insufficient adaptation to such phenological mismatches.