The Southern Ocean is home to whales, seals, seabirds and other iconic wildlife. All of these animals depend either directly, or indirectly, on a small marine prey species known as Antarctic krill, which thrives in the harsh conditions of the Southern Ocean. At night, large swarms of krill move towards the water surface to feed on plankton before returning to the depths during the day to avoid whales, fish and other predators. This synchronized movement influences the structure of the ecosystem in a number of ways by transporting carbon and influencing predator-prey interactions.

Researchers have observed the movements of krill swarms for many decades, but the processes controlling this swimming behavior remained unknown, in part, due to a lack of tools that can track the movements of individual krill. Do the krill simply respond to light and other external cues, or do they also have internal biological clocks that can maintain the observed rhythms even without such cues?

In 2024, researchers developed a new monitor known as AMAZE, which can record the swimming activity of individual krill in tanks of seawater. Hüppe et al. – including many of the researchers involved in the 2024 work – have now used this technique to trace the movement of individual wild-caught krill under different light conditions and seasons.

Hüppe et al. captured krill from the Southern Ocean on a commercial fishing boat and transferred them into a tank on the vessel for experiments. Observations revealed that the krill were most active at night, matching their natural patterns of migration in the wild. These patterns of nighttime activity adjusted to the changing length of the night over the seasons. Furthermore, the krill maintained a daily rhythm of activity even when they were kept in constant darkness for several days.

These findings suggest that an internal biological clock, in combination with light cues, regulates the swimming patterns of krill and helps them adapt to daily and seasonal changes in their environment. Understanding these internal rhythms will be key to assessing how well krill may cope with rapid changes in their environment due to climate change, which are particularly pronounced in polar regions.

Antarctic krill (Euphausia superba, hereafter referred to as krill) is a pelagic, up to 6 cm long crustacean, which is endemic to the Southern Ocean. With an estimated biomass of 300–500 million tons (Atkinson et al., 2009), krill is among the most abundant wild species worldwide (Bar On et al., 2018) and an important prey for predators such as whales, seals, and penguins (Trathan et al., 2016). Its huge abundance and central position in the food web makes krill a key species of fundamental importance for the functioning of the Southern Ocean ecosystem (Cavan et al., 2019; Trinh et al., 2023).

Krill is mostly found in swarms, the largest of which can be hundreds of meters long and tens of meters in height, likely reflecting a behavioral adaptation to minimize the risk of predation (Tarling et al., 2009; Hamner and Hamner, 2000). Along with their pronounced swarming behavior, krill display diel vertical migration (DVM), a common behavior among many pelagic zooplankton organisms across different taxa found in all oceans (Bandara et al., 2021). DVM is commonly characterized by an ascent to the surface layers in the dark of the night to feed and a descent to darker parts of the water column during the day to avoid visually hunting predators (Bandara et al., 2021; Hays, 2003). The regular, synchronized movement of this large biomass significantly shapes the structure of ecosystems (Nichols et al., 2022) and has large impacts on biogeochemical cycles (Aumont et al., 2018; Archibald et al., 2019). This includes the recycling of nutrients, stimulation of primary production, as well as transport and storage of carbon in the deep ocean (Cavan et al., 2019). Although such a ‘regular’ DVM pattern has been commonly observed for krill swarms (Godlewska, 1996; Everson, 1983), there is considerable behavioral variation, including reverse DVM, higher frequency migrations, or no synchronized migrations at all (Godlewska, 1996; Bahlburg et al., 2023b). While the adaptive advantage of balancing increased predation pressure during the day with the need to feed seems obvious, the underlying mechanisms of DVM and its modulations are not understood. Light is thought to be the most reliable and thus important environmental cue for DVM (Ringelberg and Van Gool, 2003). However, a study in the marine copepod Calanus finmarchicus indicates that DVM behavior is underpinned by a circadian clock, which helps the animals to adjust behavior, physiology, and gene expression to the day-night cycle (Häfker et al., 2017). Similarly, a study on Norwegian krill, Meganyctiphanes norvegica, suggested swimming activity in krill is under clock control, with increased activity during the dark phase (Velsch and Champalbert, 1994). In Antarctic krill, similar studies have been conducted to test the hypothesis of a clock involvement in DVM behavior (Gaten et al., 2008; Piccolin et al., 2020). While these studies gave first hints that daily behavioral activity in krill is partly under endogenous control, a large variability hindered a clear characterization of the circadian behavioral activity of krill.

Previous studies on endogenous rhythms in krill identified the molecular components of a krill circadian clock (Biscontin et al., 2017; Shao et al., 2023). It has further been shown that the krill circadian clock drives daily rhythms in gene expression, metabolism, and behavior (Piccolin et al., 2020; Teschke et al., 2011; Biscontin et al., 2019). Part of krill’s success lies in its strong adaptation to the extreme seasonality of the Southern Ocean environment (Ducklow et al., 2007), which is reflected in a fundamental, seasonal regulation in body composition, metabolic activity, feeding, growth (Meyer et al., 2010; Quetin and Ross, 1991), sexual maturity (Kawaguchi et al., 2007; Siegel, 2012), and gene expression (Seear et al., 2012; Höring et al., 2021). Results from laboratory studies showed that photoperiod is a major driver for seasonal ecophysiological changes in krill (Brown et al., 2011; Höring et al., 2018; Teschke et al., 2007), and it has been suggested that an endogenous timekeeping system (i.e. biological clock) is involved, which uses photoperiod as a synchronizing cue (Höring et al., 2018; Piccolin et al., 2018b).

Circadian clocks are widespread and well-studied endogenous timing mechanisms which allow an organism to fine-tune biological functions to specific times of the day-night cycle. The endogenous oscillation is produced by transcriptional-translational feedback loops of a set of clock genes and their translation products (Tomioka and Matsumoto, 2010), which, under the absence of external cues, produce a temporal signal with a period (τ) of about 24 hr. Under natural conditions, the rhythm of the central oscillator is synchronized to exactly 24 hr by predictable environmental cycles, called zeitgeber, of which light is usually the most important (Roenneberg et al., 2003). The rhythmic signal of the central oscillator is superimposed on downstream processes, which results in the temporal regulation of several biological functions, such as gene expression, physiology, and behavior. Thus, the circadian clock allows organisms to anticipate daily environmental cycles and adapt their biology, ultimately increasing survival and fitness (Krittika and Yadav, 2020). Since the circadian clock implicitly measures day length, it is also capable of providing seasonal information. Consequently, the circadian clock has also been shown to be involved in the timing of seasonal functions, such as the induction of reproduction or diapause (Saunders, 2020; Helfrich-Förster, 2024).

While most knowledge about circadian clocks and their involvement in organism’s daily and seasonal processes stems from terrestrial model organisms, little is known about clocks in the marine environment (Tessmar-Raible et al., 2011). This is especially true for marine habitats in polar regions, characterized by extreme photic conditions, including polar night and midnight sun phases. An understanding of the mechanistic underpinnings of biological timing is essential to comprehend how organisms adapt to their specific environment. This is particularly important in times of rapid environmental change, which can alter the temporal synchronization of trophic interactions, including DVM, feeding, and swimming behavior, and, thus, the functioning of whole ecosystems (Helm et al., 2013).

In this study, we use the novel Activity Monitor for Aquatic Zooplankter (AMAZE) (Hüppe et al., 2024) to investigate the mechanistic basis of swimming activity of wild-caught Antarctic krill under controlled environmental conditions onboard a commercial krill fishing vessel. We provide novel evidence that the circadian clock underlies ecologically important behaviors, such as DVM, and discuss how the krill circadian clock could control the timing of seasonal life cycle functions in krill.

Two sets of experiments were conducted for this study (Figure 1). In the first set of experiments (experiment 1) we adopt a standard chronobiological experiment design, where we monitor krill behavioral activity under simulated short days (short-day treatment) or long days (long-day treatment), before they are transferred into constant darkness for several days to investigate the influence of a circadian clock on krill behavior. In a second set of experiments (experiment 2) krill vertical migration behavior in the field was recorded for several days before sampling and transferring krill into constant darkness. This experiment was conducted in four seasons (summer treatment, late summer treatment, autumn treatment, and winter treatment).

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A circadian clock is involved in the daily regulation of swimming activity

To investigate whether a circadian clock is involved in regulating daily rhythms of swimming activity, we sampled krill from the field under short-day conditions in winter (short-day treatment, sampling date: May 31, 2021, local photoperiod: 5.5 hr) and under long-day conditions in late summer (long-day treatment, sampling date: February 16, 2022, local photoperiod: 15.3 hr; see Table 1 for details). We exposed 11 and 9 sampled individuals to 3 days of light-dark conditions in the activity monitor simulating short-day conditions and to 5 days of LD simulating long-day conditions, respectively. The photoperiod in the activity monitor approximated the natural photoperiod in the field during sampling. The period of LD was followed by 5 days of constant darkness. The data under LD conditions show that krill swimming activity at both individual and group level increased during the dark phase and showed a strong synchronization with the light-dark cycle provided (Figure 2—figure supplements 1 and 2).

Table 1

Experiment ID	Experimental light regime	Experiment duration (days)	Sampling date (UTC-2)	Sampling time (UTC-2)	Sampling region	Sampling location (latitude °S/longitude °W)	Sampling depth (m)	Natural photoperiod (hr)	n Krill (total/male/ female)	Mean ±SD length (mm)
Experiment 1 (short-day treatment)	LD-DD	3 (LD), 5 (DD)	2021-05-31	13:02	BS	62.95/57.77	170	5.5	11/5/6	45±2.6
Experiment 1 (long-day treatment)	LD-DD	5 (LD), 5 (DD)	2022-02-16	15:50	SOI	60.04/46.45	94	15.3	9/4/5	44.4±3.7
Experiment 2 (summer treatment)	DD	8	2022-01-22	17:03	SOI	60.08/46.46	157	17.5	9/8/1	42.4±1.5
Experiment 2 (late summer treatment)	DD	6	2022-03-01	11:00	SOI	60.0/44.73	86.5	14.0	9/4/5	48.9±4.4
Experiment 2 (autumn treatment)	DD	7	2022-03-15	08:40	SOI	60.28/46.43	119.2	12.6	10*/4/5	51.3±1.6*
Experiment 2 (winter treatment)	DD	4	2021-06-10	12:56	SOI	60.5/46.11	185	5.9	9/2/7	49.2±3.9

1. *

   Length and sex of one individual undetermined.

As synchronization between individuals and robustness of activity patterns under DD within individuals was strongest in krill from the short-day treatment, we used these data for initial assessments of circadian activity rhythms. Under constant darkness conditions in the short-day treatment, krill swimming activity continued in several individuals (n=6; 54%) with significant circadian rhythmicity over the 5 days of DD conditions (Figure 2a and b, Figure 2—figure supplement 3), indicating the involvement of a circadian clock in the daily regulation of swimming activity. Nevertheless, in most individuals, the amplitude of the rhythm decreased over time (Figure 2a, Figure 4a, Figure 2—figure supplement 3). The patterns of swimming activity observed at the individual level were reflected at the group level, showing a strong synchronization of increased swimming activity with the dark phase under light-dark conditions (Figure 3a, Figure 2—figure supplement 1), and persistent significant circadian swimming activity under constant conditions with a continuously decreasing amplitude throughout the experiment (Figure 2c and d; Figure 4a: paired t-test, p-value=0.005, Figure 4c: paired t-test, p-value=0.012).

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Figure 4

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Circadian swimming activity persists with a stable phase after entrainment to a wide range of natural photoperiods

To gain insights into potential seasonal differences in the regulation of krill swimming activity, we sampled krill from the field in summer (summer treatment), late summer (late summer treatment), autumn (autumn treatment), and winter (winter treatment) and recorded their swimming activity for 4–8 days under constant darkness conditions, without previous entrainment in the activity monitor (see Table 1 for details).

Similar to our previous analysis of individual krill swimming activity under constant darkness conditions, a large proportion of the recorded individuals in each experiment (44–100%) exhibited significant rhythmicity in the circadian range (Figure 5—figure supplements 1–4), which is also reflected in rhythmic swimming activity at the group level (Figure 5a–d, Figure 5—figure supplement 5). Interestingly, the pattern of circadian swimming activity, with two peaks during the dark phase, appears to become clearer and higher in amplitude with shortening photoperiods toward winter (Figure 5a–d). This is supported by rhythm analysis of the group behavior, which revealed a higher power and a period estimation closer to 24 hr with shortening photoperiod (Figure 5—figure supplement 6). While the morning peak is mainly visible in autumn and winter, the late-night activity peak is visible throughout the year, at the same time of the subjective 24 hr-day (Figure 5e–h). This pattern appears irrespective of the natural photoperiod the animals were entrained to in their natural environment before they were sampled for the respective experiment.

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Synchronized DVM in the field is present across a wide range of natural photoperiods

To investigate whether krill swarms exhibited daily behavioral patterns in swimming behavior in the field before they were sampled for seasonal experiments, hydroacoustic data were recorded from the fishing vessel, continuously over a 3-day period prior to sampling for the seasonal experiments described above (for vessel positions during hydroacoustic recordings, see Figure 1—figure supplement 1). The data provide information about the vertical distribution of krill swarms in the upper water column (<220 m) below the vessel over time (Figure 6a–d). The hydroacoustic data in summer, late summer, and autumn show that krill swarms performed DVM, highly synchronized with the local light regime (Figure 6a–c). The swarms regularly ascended to the surface layers (<50 m) around sunset and returned to deeper layers (>100 m) around sunrise. In winter, little signal is visible in the upper water layer, indicating very low density or the absence of krill swarms (Figure 6d). Consequently, krill for the winter treatment was sampled from deeper waters (185 m). This agrees with observations that krill shift their distribution to deeper waters in winter, where krill have been observed to perform DVM also during this time of year (Bahlburg et al., 2023b). The available data only covers the upper 220 m of the water column, meaning that the dynamics of swarms below this depth are missed.

Figure 6

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Our study revealed continued rhythmic swimming activity under constant darkness, showing the involvement of a circadian clock in swimming behavior of krill, as has been previously shown for other marine pelagic crustaceans (Häfker et al., 2017; Velsch and Champalbert, 1994; Cohen and Forward, 2005). To date, only three studies have investigated the involvement of a circadian clock in the regulation of swimming behavior in krill species, including E. superba (Gaten et al., 2008; Piccolin et al., 2020) and M. norvegica (Velsch and Champalbert, 1994). Data from Piccolin et al., 2020, showed a strong damping of the amplitude and indication of a remarkably short (~12 hr) free running period (FRP) of vertical swimming behavior of a group of krill under constant darkness (Piccolin et al., 2020). The short period found in Piccolin et al., 2020, is in line with our findings of a bimodal activity pattern under DD conditions on the individual level, suggesting that the ~12 hr rhythm in group swimming behavior in Piccolin et al., 2020, could have resulted from a bimodal activity pattern at the individual level, as found in our study. Bimodal locomotor activity rhythms are well known across different species, possibly most prominently in the fruit fly (Drosophila melanogaster), where two coupled endogenous oscillators control morning and evening activity bouts (Helfrich-Förster, 2001). In our experiments, we observed a strong weakening of the evening activity under constant conditions, especially after entrainment to long days, while the late-night activity peak appeared more robust. The differential variation in the morning and late-night activity suggests that the circadian activity bouts could also be controlled separately at the neuronal level in krill.

Comparing the daily pattern of swimming activity under LD conditions with those under DD, it is clear that the amplitude of the rhythm was significantly higher under LD than under DD. In addition, the activity under LD was organized into three activity phases, one in the evening, one late at night, and a smaller one in the morning. In contrast, under DD there were a maximum of two activity phases during the subjective night. Light is known to play a dual role in regulating daily behavioral activity. On the one hand, light functions as a zeitgeber, which synchronizes the circadian clock with the day-night cycle, a process called entrainment (Aschoff, 1960).

On the other hand, it can directly affect clock output functions such as physiology and behavior, known as masking (Aschoff, 1960; Mrosovsky, 1999). The masking response depends on the activity type of the organism, and light was shown to promote activity in diurnal animals while inhibiting activity in nocturnal ones (Aschoff and von Goetz, 1989; Aschoff and von Goetz, 1988). Krill are regularly observed performing nocturnal DVM (Godlewska, 1996; Everson, 1983), including in the present study, with higher activity during the night, including the times of twilight, related to foraging and feeding activity and vertical ascend and descend movements (Zhou and Dorland, 2004; Klevjer and Kaartvedt, 2011). The observed effect of light on reducing krill swimming activity under LD conditions in our study is thus in line with previous concepts of the exogenous effects of light on nocturnal organisms (Aschoff, 1960; Mrosovsky, 1999). However, under LD conditions, the observed swimming activity pattern in krill is not solely driven by light. The increase in activity in the evening and the second half of the dark phase under LD conditions flexibly adjusts to the length of the night and seems to persist under constant darkness, suggesting these bouts to be under clock control, as discussed above.

The reduced amplitude in swimming activity after the switch to DD conditions and further damping of amplitude over time under constant darkness has been found in other studies in krill (Piccolin et al., 2020) and other marine zooplankton organisms (Häfker et al., 2017; Cohen and Forward, 2005). A rapidly damping output signal under constant conditions could indicate a weak, low amplitude circadian oscillator, where the damping amplitude of the clock output signal is caused by a rapid desynchronization of clock neurons, when zeitgeber signals are absent (Webb et al., 2012). Interestingly, weak oscillators have been found in different fruit fly species (Bertolini, 2019; Beauchamp et al., 2018), the Svalbard reindeer (Arnold et al., 2018), and Svalbard ptarmigan (Appenroth et al., 2021), native to high latitudes and species that exhibit pronounced seasonal rhythmicity, such as aphids (Beer et al., 2017; Barberà et al., 2017). It is known that weaker clocks are more flexible and can be entrained more efficiently than those that are more rigid and self-sustained (Webb et al., 2012; Abraham et al., 2010). This could confer a significant adaptive advantage to species inhabiting environments characterized by extreme photic conditions (Bertolini, 2019; Beauchamp et al., 2018; Bloch et al., 2013), such as phases of polar night or midnight sun as well as rapid changes in day length, or species that rely on precise photoperiodic time measurement for accurate seasonal adaptation. In the Southern Ocean, photoperiod becomes extreme around the solstices, and its daily change is rapid around the spring and autumn equinoxes. A weak oscillator could, therefore, ensure that krill remains synchronized with the extreme and rapidly changing photic conditions and, thus, its environment.

Indeed, our data from activity recordings under DD conditions of krill sampled in different seasons indicate persistent circadian swimming activity, irrespective of the season. Our findings suggest that the krill circadian clock remains functional and drives rhythmic behavioral output in natural conditions throughout the year. This finding is complemented by the hydroacoustic recordings in the days preceding krill sampling for activity experiments. In summer, late summer, and autumn, krill swarms exhibited apparent DVM behavior, synchronized to the natural photoperiod. While we did not observe DVM in the upper water column during sampling in winter, acoustic recordings from other studies in winter indicate that krill may perform DVM also in winter (Cisewski et al., 2010), potentially in deeper layers.

Our data show that light acts in concert with, and is likely modulated by, the circadian clock to achieve the observed daily regulation in krill swimming activity. Nevertheless, further studies at the behavioral, molecular, and neuronal levels are required to elucidate the endogenous and exogenous effects of light and the circadian clock on the different behavioral aspects observed and to gain further insights into the characteristics of the molecular mechanism of the krill clock.

In a high-latitude region, such as the Southern Ocean, the timing of crucial life history functions to seasonal fluctuations of light, food availability, and sea ice extent is key to organisms’ success. In contrast to early studies, which suggested that only food availability was the main driver of krill’s seasonal physiological functions (Ikeda and Dixon, 1982), later studies have revealed that photoperiod, likely in concert with circannual timing, drives the seasonal regulation of key life cycle functions (Meyer et al., 2010; Brown et al., 2011; Höring et al., 2018; Teschke et al., 2007; Piccolin et al., 2018b).

Although the exact molecular mechanism of seasonal timing remains unknown, there is clear evidence that the circadian clock measures day length and provides information about the seasonal progression (Saunders, 2020; Helfrich-Förster, 2024). Several studies in insects (Saunders, 2024) and plants (Vicentini et al., 2023) support the external coincidence model (Pittendrigh and Minis, 1964). This model explains how the circadian clock regulates the expression of a light-sensitive substance during the late dark phase. Under long days, this substance is degraded by morning light, suppressing a winter response, while the substance accumulates under short days (and long nights), inducing a winter-like response. In the case of krill, this response could include sexual regression, increased lipid accumulation (Kawaguchi et al., 2007; Höring et al., 2018), and a reduction in overall metabolism (Meyer et al., 2010; Piccolin et al., 2018b).

Our data on krill circadian swimming activity of animals sampled from the field in different seasons show a remarkably stable peak in late-night activity (Figure 5e–h). Assuming that the behavioral activity under constant darkness reflects the direct influence of the circadian clock, our findings suggest that the krill circadian clock can measure the length of the day (or night) via external coincidence. The increased rhythmicity and synchronization of animals under shortening photoperiods indicate the potential of precise day length measurement especially during seasonal physiological changes (Meyer et al., 2010). The day length information could subsequently be used directly to synchronize physiological functions with the environment and/or indirectly to entrain a circannual clock (Miyazaki, 2023), which subsequently drives rhythmic annual output. While the individual activity recordings provide first insights into potential mechanisms for the control of daily and seasonal processes in krill, it must be noted that behavioral output does not always reflect the detailed characteristics of the circadian oscillator (Häfker et al., 2024). Further investigations into the molecular clock mechanism and its downstream functions across seasons are needed to clarify the involvement of the circadian clock in photoperiodism and circannual rhythms in krill.

Circadian clocks have the potential to anticipate the daily light-dark cycle and thereby enable a fine-tuned synchronization of behavioral and physiological functions with environmental cycles, which increases an organism’s fitness (Krittika and Yadav, 2020). Consequently, synchronizing krill behavioral output with the day-night cycle provides potential adaptive advantages on various levels.

DVM of zooplankton seems to be a trade-off between predation risk and feeding (Ringelberg and Van Gool, 2003). As it is complex to directly sense predation risk, light is a robust proxy (Benoit Bird and Moline, 2021) and a circadian clock provides an additional mechanism to anticipate and synchronize the times of vertical migration, active feeding, and foraging with nighttime. Our data show that light, in addition to the clock, ensures robust, synchronized activity patterns. Differences between entrained and free running conditions further indicate that evening and late-night activity are under clock control. At the same time, the activity peak in the morning is a response to the onset of light. A differential regulation of certain phases of DVM has previously been suggested for marine zooplankton species (Häfker et al., 2017; Cohen and Forward, 2005). A clock-driven evening ascent would allow for the anticipation of sunset and thus the timely initiation of migration when krill swarms are in deeper water layers, resulting in optimized surface feeding time. The clock-controlled late-night activity could support a second feeding bout and preparation for a timely morning descent before sunrise increases visual predation risk. Interestingly, the decrease in clock-controlled swimming activity during the early night, right after the evening activity bout, may further facilitate a phenomenon called ‘midnight sinking’, which describes the sinking of animals to intermediate depths after the evening ascent, followed by a second rise to the surface before the morning descend. This behavior has been observed in a number of zooplankton species, including calanoid copepods (see Tarling et al., 2002; Cushing, 1951 and references therein) and krill (Tarling and Johnson, 2006). While previous studies suggested several exogenous factors, such as satiation or predator presence, as drivers of the midnight sink (Tarling et al., 2002; Cushing, 1951), our study suggests that this pattern may be partly under endogenous control. In situ hydroacoustic observations have demonstrated increased swimming speeds during nighttime for both M. norvegica and E. superba (Zhou and Dorland, 2004; Klevjer and Kaartvedt, 2011). This increase is likely related to active foraging and feeding behavior, as higher swimming speeds increase the chance of encountering food particles and thus increase food uptake. Nevertheless, swimming in krill is energetically costly and can make up more than 70% of the total energy expenditure (Kils, 1981). Reducing swimming activity to the baseline level during the day thus represents a significant opportunity for energy conservation.

At high latitudes, biological clocks are exposed to extreme changes in photoperiod throughout the year, including phases of midnight sun and polar night. Many organisms inhabiting polar regions show arrhythmicity, at least during parts of the year, and potential mechanisms include direct impacts on the central oscillator and uncoupling between output functions and the circadian clock (Bloch et al., 2013). Previous investigations of krill clock gene expression in the laboratory indicated a weaker oscillation of the krill clock and metabolic output functions under simulated extreme photic conditions (i.e. LL and LD 3:21), compared to more balanced day-night cycles (Piccolin et al., 2018a). Data on the transcriptomic and organismic level further indicate that krill can flexibly adapt to the photic conditions at different latitudes (Höring et al., 2021; Höring et al., 2018). This aligns with our findings, where krill, sampled across a wide range of photoperiods, remain behaviorally synchronized with the local photoperiod under entrained conditions, but show reduced endogenous rhythmicity under DD after entrainment to long-day conditions. Krill inhabits a broad range of latitudes, including regions with clear day-night cycles and regions with polar night and midnight sun during the seasonal extremes (Siegel et al., 2016). At the same time krill is transported rapidly between regions via ocean currents (Fach et al., 2006), potentially exposing the same individuals to various photic conditions during their life span. A weak circadian clock in close interaction with the ambient light regime could thus allow krill to adopt the best strategy for the environmental conditions prevailing in the current location. For example, at high latitudes, the adaptive advantage of predator evasion with DVM diminishes in summer when the upper water column is illuminated constantly. In this case, arrhythmic behavior would allow flexibly exploiting food patches at any time of day, when the need for food is high to fuel reproductive processes (Quetin and Ross, 2001). Further, a study on the marine annelid Platynereis dumerilii recently highlighted a differential regulation of clock-controlled processes, where behaviorally arrhythmic individuals show increased rhythmicity in physiological output (Häfker et al., 2024), indicating the possibility of flexibly adapting timed processes to environmental conditions.

Adapting to a fluctuating environment involves significant seasonal physiological changes in krill to survive the harsh, food-scarce winter (Meyer et al., 2010; Meyer, 2012). Crucial processes, such as accumulating enough lipids, must begin long before winter, requiring an anticipatory mechanism. Recent evidence suggests that photoperiod and circannual timing drive these seasonal changes in krill physiology, using photoperiod as a proxy for seasonal progression (Meyer et al., 2010; Brown et al., 2011; Höring et al., 2018; Teschke et al., 2007; Piccolin et al., 2018b). Rapid warming in the Southern Ocean is observed to cause shifts in phytoplankton bloom timing (Thomalla et al., 2023), which may lead to temporal mismatches between photoperiod synchronized krill physiology and their primary food source, with the potential to reduce reproductive success (Helm et al., 2013) and negatively impact the krill-dependent ecosystem. Understanding the mechanistic basis of species adaptation and their flexibility is therefore crucial in times of rapid environmental change (Helm et al., 2013).

We used a new krill activity monitor to identify the endogenous underpinnings of swimming activity of wild-caught Antarctic krill. The results of our experiments provide clear evidence that a circadian clock underlies krill behavior, driving a distinct bimodal pattern of clock-controlled swimming activity. The damping of the activity amplitude under constant darkness suggests that krill possess a ‘weak’, highly flexible circadian clock adapted to a life under extreme and variable conditions. These findings are further supported by experiments conducted under simulated short-day and long-day conditions, demonstrating a flexible adaptation of the krill swimming activity pattern to a wide range of photoperiods. The results provide novel insights into the combined impacts of the circadian clock and light on the daily regulation of swimming activity. Furthermore, hydroacoustic recordings demonstrate that most krill swarms sampled exhibited synchronized DVM in the field in the days directly before sampling for behavioral experiments, indicating that in this region, krill remain behaviorally synchronized across a wide range of photoperiods. Seasonal recordings of field-entrained circadian swimming activity suggest that the krill circadian clock may be involved in measuring day length and, consequently, the timing of seasonal events. The findings provide novel insights into the mechanistic underpinnings of daily and seasonal timing in Antarctic krill, a marine pelagic key species, endemic to a high-latitude region. Mechanistic studies are a prerequisite for understanding how krill adapt to their specific environment and their flexibility in responding to environmental changes.

The datasets and analysis scripts used for the analysis of krill swimming activity, as well as of hydroacoustic recordings are available in Zenodo.

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Author details

1. Lukas Hüppe

   1. Neurobiology and Genetics, University of Würzburg, Biocenter, Theodor-Boveri-Institute, Würzburg, Germany
   2. Section Polar Biological Oceanography, Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Bremerhaven, Germany

   Contribution

   Conceptualization, Data curation, Formal analysis, Visualization, Methodology, Writing – original draft, Writing – review and editing

   For correspondence

   lukas.hueppe@uni-wuerzburg.de

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7793-9046

2. Dominik Bahlburg

   Section Polar Biological Oceanography, Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Bremerhaven, Germany

   Contribution

   Visualization, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0210-0649

3. Ryan Driscoll

   National Oceanography Centre, European Way, Southampton, United Kingdom

   Contribution

   Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

4. Charlotte Helfrich-Förster

   Neurobiology and Genetics, University of Würzburg, Biocenter, Theodor-Boveri-Institute, Würzburg, Germany

   Contribution

   Conceptualization, Supervision, Funding acquisition, Methodology, Project administration, Writing – review and editing

   Competing interests

   No competing interests declared

5. Bettina Meyer

   1. Section Polar Biological Oceanography, Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Bremerhaven, Germany
   2. Institute for Chemistry and Biology of the Marine Environment, University of Oldenburg, Oldenburg, Germany
   3. Helmholtz Institute for Functional Marine Biodiversity at the University of Oldenburg (HIFMB), Oldenburg, Germany

   Contribution

   Conceptualization, Supervision, Funding acquisition, Project administration, Writing – review and editing

   For correspondence

   bettina.meyer@awi.de

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-6804-9896

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