Antarctic krill, Euphausia superba, a model organism to study the mechanisms of temporal physiological and behavioral synchronization of polar pelagic organisms
Antarctic krill is a shrimp-like crustacean species which shapes the structure of the Southern Ocean ecosystem due to its central position as direct link between primary producers and apex predators such as whales, seals, penguins and many fish species. A decline in winter sea ice duration caused by climatic warming resulted in a long-term decline in krill biomass in the Scotia Sea sector of the Southern Ocean . Krill’s central position in the food web, the ongoing environmental changes in its habitat, and increasing commercial interest emphasize the urgency of understanding the adaptability of krill to its environment . Krill has evolved rhythmic physiological and behavioral functions which are synchronized with the daily and seasonal cyclic changes of the Southern Ocean ecosystem. These occur over a daily cycle, such as diel vertical migration (DVM), which is believed to allow krill to maximize food intake in the upper water column during the night and minimize predator risk in the deep during the day . In addition, krill exhibits seasonal cycles of metabolic regulation and maturity which are synchronized with the extreme seasonal cycles in environmental factors such as day length, sea ice extent and food availability [3,4,11,12].
During the last 10 years, the krill group at AWI has contributed significant findings in understanding the nature of these daily and seasonal cycles. In the first instance, seasonal investigations, both field based and in the laboratory, revealed that important physiological functions of krill such as metabolic activity, feeding and growth [3,12,13], as well as maturity  are affected by different light-dark cycles, irrespective of food supply, suggesting that the photoperiod acts as the main Zeitgeber for these annual cycles. These adaptations could therefore represent an endogenous adaptational strategy that is controlled by an endogenous timing system in krill and synchronized by the seasonal course of photoperiod in the environment. Indeed, recent investigations have reinforced this suggestion. In cooperation with the CUB (chronobiology lab of Prof. A. Kramer) the first report of an endogenous circadian timing system in Antarctic krill and evidence for its link to metabolic key processes has been identified . It is very likely that this system is essential for krill as it facilitates synchronization of its physiology and behavior to daily environmental cycles but may also play a role for the control of seasonal events during its annual life cycle. However, in general our understanding of how circadian clocks of high latitude organisms such as krill might have adapted to the strong variability in annual day length that at the extreme may ranges from constant darkness in winter to constant light in summer is small. Polar organisms might show a wide plasticity of the circadian clock machinery that enable them to cope with prolonged periods without the presence of a strong Zeitgeber either by adopting arrhythmic behaviour or by switching to alternative environmental cues. Also additional endogenous timing mechanisms may play an important role as long-term simulative photoperiod experiments with live krill suggests the presence of a circannual timing mechanism . Synchronization between krill and its environment may therefore depend upon a complex interplay between internal clocks (circadian/circannual), which control circadian phenotypes and also may modulate photoperiodic responses, and different environmental cues. Biological timing in Antarctic krill, its underlying mechanisms, and its functional interaction with the external environment are still not fully understood.
These studies and the developed research network represent a large step forward in understanding the mechanisms of temporal synchronization in a key Southern Ocean species. The HVI PolarTime, will lead to the first comprehensive analyses of the circadian clock of a polar marine organism. At the same time, krill will act as model organism to study how the circadian clock and/or additional endogenous timing systems mediate daily and seasonal life-cycle functions and how these clocks and rhythms interact with environmental parameters. This offers a unique opportunity to study whether a single or multiple clocks have evolved. Accordingly, this can elucidate how a single clock can generate outputs with multiple periodicities; or how different clocks can co-exist and interact one with another. This will act as a solid basis to study and understand the mechanisms of temporal synchronization of other key polar pelagic organisms such as calanoid copepod species.
Understanding the mechanisms of temporal synchronization of key polar pelagic organisms will be of essential importance to understand their life cycles and thus predicting the response of these species to the ongoing environmental changes. For example, throughout the year Antarctic krill undergo an endogenous reproductive cycle with a peak (full sexual maturity, reproduction) in December-January and a trough (regression of sexual maturity) in May-June. There is already strong evidence that there is a biological clock underlying this endogenous rhythm and that the seasonal course of photoperiod is an important external entrainment signal that is influencing the maturity of krill . Potential climate change scenarios may therefore cause chronological mismatches detrimental to krill population success and with profound consequences for the whole marine ecosystem:
Changes in seasonal sea ice dynamics, crucial to the amount of food available at a specific latitude.
Sea ice retreat during spring seeds the upper ocean with phytoplankton cells, and creates a low salinity, stable surface layer which leads to a substantial increase of phytoplankton concentration at the ice edge. The ovary of female krill begins to mature at this time, and the spring bloom is an important fuel for this process. The warming in the SW Atlantic sector seems to cause a later increase of sea ice extent and earlier retreat, consequently influencing the timing of the phytoplankton spring bloom. Hence, following its endogenous reproductive cycle which is influenced by the temperature independent photoperiodic cycle, krill might not be able to cover its high energetic needs in spring for its maturation and spawning processes. The previously matched interaction between the krill maturity cycle and sea ice dynamics could go out of phase and have negative consequences for its population success.
Changes in the seasonal cycle of photoperiod associated with any changes in latitude of optimal sea ice conditions.
In parallel with the warming at the northern West Antarctic Peninsula (WAP), the maritime system in this region is shifting southward along the Antarctic Peninsula, replacing the colder continental polar system of the southern WAP. Migration of krill from lower (e.g. Scotia Sea) to higher latitudes (e.g. Bellingshausen and Amundsen Seas), as already observed, implicates profound changes in the seasonal course of photoperiod. Laboratory experiments have shown that changes in photoperiod can re-entrain the clock and artificial light conditions of prolonged photoperiod can force animals into maturity while shortened photoperiods force animals into regression of maturity faster than under a natural light-dark regime [4,14]. Previously matched interaction between the krill maturity cycle and sea ice dynamics at lower latitudes can go out of phase at higher latitudes and can negatively affect recruitment success.
Changes in seawater temperature and putative direct effects on the endogenous timing system in krill.
Important physiological and behavioral functions in krill are driven by an endogenous clock machinery (i.e. circadian clock) on a transcriptional level . One highly conserved feature of circadian clocks is that their periods remain relatively constant over a physiological range of temperatures, so called temperature compensation . The temperature range in which the clock performance is temperature-compensated in polar organisms; or whether polar clocks possess an aberrant mechanism compared to temperate organisms is far from clear. With an increase in seawater temperature important features of the circadian timing system in krill may be directly affected and consequently cause chronological mismatches between environmental cycles and the physiological and behavioral performance of krill.
Despite the unique position of krill in the Southern Ocean our knowledge of the response of this species to environmental changes is lacking. In the southwest Atlantic sector the krill stock declined by 80% over the past 30 years in concert with a decline in sea ice extent and duration . However, the functional relationship between the population dynamics of krill and environmental changes is far from clear. A critical point here is that we need to progress beyond correlative studies towards a mechanistic understanding of how the life cycle of central organisms are interconnected with their environment to make predictions of future changes in polar marine environments due to the anthropogenic warming .
In this respect, the major scientific goals of PolarTime are:
- Research on endogenous timing systems and their impact on daily and seasonal physiological functions in Antarctic krill
- Investigation of the functional molecular characteristics of the circadian clock machinery of krill
- Understanding the adaptive plasticity of the endogenous clock machinery in krill
- Transfer principles to study temporal synchronization of other key polar pelagic organisms
- Embedded modeling and community ecology studies to transfer the results derived from our physiological and genetic studies in an ecosystem context to make prediction of future ecosystem changes.