Moonlight drives ocean-scale mass vertical migration of zooplankton during the Arctic winter

The creation of the pan-Arctic archive of ADCP data was supported by the UK Natural Environment Research Council (NERC) (Panarchive: NE/H012524/1 and SOFI: NE/F012381/1) as was mooring work in Svalbard (Oceans 2025 and Northern Sea Program). Moorings were also supported by the Research Council of Norway (NFR) projects: Circa (214271), Cleopatra (178766), Cleopatra II (216537), and Marine Night (226471).In extreme high-latitude marine environments that are without solar illumination in winter, light-mediated patterns of biological migration have historically been considered non-existent [1]. However, diel vertical migration (DVM) of zooplankton has been shown to occur even during the darkest part of the polar night, when illumination levels are exceptionally low [2 and 3]. This paradox is, as yet, unexplained. Here, we present evidence of an unexpected uniform behavior across the entire Arctic, in fjord, shelf, slope and open sea, where vertical migrations of zooplankton are driven by lunar illumination. A shift from solar-day (24-hr period) to lunar-day (24.8-hr period) vertical migration takes place in winter when the moon rises above the horizon. Further, mass sinking of zooplankton from the surface waters and accumulation at a depth of ∼50 m occurs every 29.5 days in winter, coincident with the periods of full moon. Moonlight may enable predation of zooplankton by carnivorous zooplankters, fish, and birds now known to feed during the polar night [4]. Although primary production is almost nil at this time, lunar vertical migration (LVM) may facilitate monthly pulses of carbon remineralization, as they occur continuously in illuminated mesopelagic systems [5], due to community respiration of carnivorous and detritivorous zooplankton. The extent of LVM during the winter suggests that the behavior is highly conserved and adaptive and therefore needs to be considered as “baseline” zooplankton activity in a changing Arctic ocean [6, 7, 8 and 9].Publisher PDFPeer reviewe

Loss of buoyancy control in the copepod Calanus finmarchicus

A mechanism is demonstrated that could explain large-scale aggregations of lipid-rich copepods in the surface waters of marine environments. Laboratory experiments establish that changes in salinity and temperature induce lipid-mediated buoyancy instability that entrains copepods in surface waters. Reduced hydrostatic pressure associated with forced ascent of copepods at fjordic sills, shelf breaks and seamounts would also reduce the density of the lipid reserves, forcing copepods and particularly those in diapause to the surface. We propose that salinity, temperature and hydrodynamics of the physical environment, in conjunction with the biophysical properties of lipids, explain periodic high abundances of lipid-rich copepods in surface waters

Calanus finmarchicus seasonal cycle and diapause in relation to gene expression, physiology, and endogenous clocks: Calanus finmarchicus seasonal rhythmicity

The copepod Calanus finmarchicus plays a crucial role in the north Atlantic food web. Its seasonal life cycle involves reproduction and development in surface waters before overwintering in diapause at depth. Although diapause has been studied for more than a century, the factors responsible for the initiation and termination of it are still unclear. Endogenous clocks have been identified as potent tools for photoperiod measurement and seasonal rhythmicity in many terrestrial species, but knowledge of these remains scarce in the marine realm. Focusing on the dominant CV copepodid stage, we sampled a population of C. finmarchicus from a Scottish sea loch to characterize population dynamics, several physiological parameters, and diel and seasonal expression rhythms of 35 genes representing different metabolic pathways, including the circadian clock machinery. This generated a detailed overview of the seasonal cycle of C. finmarchicus including the most extensive field dataset on circadian clock gene expression in a marine species to date. Gene expression patterns revealed distinct gene clusters upregulated at different phases of the copepod's seasonal cycle. While diel clock cycling was restricted to the active spring/summer phase, many clock genes exhibited the highest expression during diapause. Our results provide new insights into diapause on physiological and genetic levels. We suggest that photoperiod, in interaction with internal and external factors (lipid content, temperature, food availability) and the endogenous clock mechanism, plays an important role in the timing of diapause in C. finmarchicus

Circadian Clock Involvement in Zooplankton Diel Vertical Migration

Biological clocks are a ubiquitous ancient and adaptive mechanism enabling organisms to anticipate environmental cycles and to regulate behavioral and physiological processes accordingly [1]. Although terrestrial circadian clocks are well understood, knowledge of clocks in marine organisms is still very limited [2, 3, 4, 5]. This is particularly true for abundant species displaying large-scale rhythms like diel vertical migration (DVM) that contribute significantly to shaping their respective ecosystems [6]. Here we describe exogenous cycles and endogenous rhythms associated with DVM of the ecologically important and highly abundant planktic copepod Calanus finmarchicus. In the laboratory, C. finmarchicus shows circadian rhythms of DVM, metabolism, and most core circadian clock genes (clock, period1, period2, timeless, cryptochrome2, and clockwork orange). Most of these genes also cycle in animals assessed in the wild, though expression is less rhythmic at depth (50–140 m) relative to shallow-caught animals (0–50 m). Further, peak expressions of clock genes generally occurred at either sunset or sunrise, coinciding with peak migration times. Including one of the first field investigations of clock genes in a marine species [5, 7], this study couples clock gene measurements with laboratory and field data on DVM. While the mechanistic connection remains elusive, our results imply a high degree of causality between clock gene expression and one of the planet’s largest daily migrations of biomass. We thus suggest that circadian clocks increase zooplankton fitness by optimizing the temporal trade-off between feeding and predator avoidance, especially when environmental drivers are weak or absent [8]

Photoperiodism and overwintering in boreal and sub-Arctic Calanus finmarchicus populations

The copepod Calanus finmarchicus, a key species in the North Atlantic, generally spends the non-productive season by descending into deep waters and entering diapause, a physiological state characterized by reduced metabolism and arrested development. In the open ocean, overwintering depths are below 600 m, where temperature and light conditions are favourable to initiate diapause. However, C. finmarchicus has also been reported diapausing in areas with shallow water depth such as fjords, coastal waters and shelf seas. In these environments, the temperature and light conditions are different, and it has been hypothesized that under such conditions C. finmarchicus may remain active throughout winter. Here, we investigated changes in the swimming activity of C. finmarchicus from shallow fjords in the eastern North Atlantic during overwintering in response to ambient photoperiod. We conducted monthly experiments with populations from 2 fjords from different latitudes (sub-Arctic Ramfjord, 69°N and boreal Loch Etive, 56°N), measuring the locomotor activity of individual C. finmarchicus stage CVs exposed to a natural light:dark cycle. At both locations, peaks in activity in response to the light cycle were observed to shift from nocturnal during the early overwintering phase to diurnal during mid and late overwintering phase, with a minimal intensity observed during the mid-overwintering phase. In Ramfjord, activity and rhythmicity were generally lower than in Loch Etive. We conclude that C. finmarchicus remains active throughout its overwintering period when in shallow (<200 m) locations but down-regulates its locomotor activity during the main overwintering phase, which we describe as a winter resting state as distinct from classical diapause

Uptake of sympagic organic carbon by the Barents Sea benthos linked to sea ice seasonality

On Arctic shelves, where primary production occurs in both the pelagic and sympagic (ice-associated) habitats, sympagic organic material (OM) can constitute a disproportionate fraction of benthic diets due to higher sinking rates and lower grazing pressure than pelagic OM. Less documented is how sympagic OM assimilation across feeding guilds varies seasonally and in relation to sea ice duation. We therefore investigated the relative abundance of sympagic vs pelagic OM in Barents Sea shelf megabenthos in the summer and winter of 2018 and 2019, from 10 stations where sea ice duration ranged from 0 to 245 days per year. We use highly branched isoprenoids, which are lipid biomarkers produced with distinct molecular structures by diatoms in sea ice and the water column, to determine the ratio of sympagic-to-pelagic OM assimilated by benthic organisms. From 114 samples of 25 taxa analysed, we found that the proportion of sympagic OM assimilated ranged from 0.4% to 95.8% and correlated strongly (r2 = 0.754) with the duration of sea ice cover. The effect of sea ice duration was more evident in fauna collected during summer than winter, indicating that sympagic signals are more evident in the summer than in the winter at higher latitudes. Our data show that sympagic production can supply a high fraction of carbon for Barents Sea benthos, although this is highly variable and likely dependent on availability and patchiness of sympagic OM deposition. These results are comparable to similar studies conducted on benthos in the Pacific Arctic and highlight the variable importance of sympagic OM in the seasonal ice zone of Arctic inflow shelves, which are the Arctic regions with highest rates of sea ice loss.publishedVersio

Widely rhythmic transcriptome in Calanus finmarchicus during the high Arctic summer solstice period

Solar light/dark cycles and seasonal photoperiods underpin daily and annual rhythms of life on Earth. Yet, the Arctic is characterized by severalmonths of permanent illumination (‘‘midnight sun’’). To determine the persistence of 24h rhythms during the midnight sun, we investigated transcriptomic dynamics in the copepod Calanus finmarchicus during the summer solstice period in the Arctic, with the lowest diel oscillation and the highest altitude of the sun’s position. Here we reveal that in these extreme photic conditions, a widely rhythmic daily transcriptome exists, showing that very weak solar cues are sufficient to entrain organisms. Furthermore, at extremely high latitudes and under sea-ice, gene oscillations become re-organized to include <24h rhythms. Environmental synchronization may therefore be modulated to include non-photic signals (i.e. tidal cycles). The ability of zooplankton to be synchronized by extremely weak diel and potentially tidal cycles, may confer an adaptive temporal reorganization of biological processes at high latitudes

Behavioural and physiological impacts of low salinity on the sea urchin Echinus esculentus

Reduced seawater salinity as a result of freshwater input can exert a major influence on the ecophysiology of benthic marine invertebrates, such as echinoderms. While numerous experimental studies have explored the physiological and behavioural effects of short-term, acute exposure to low salinity in echinoids, surprisingly few have investigated the consequences of chronic exposure, or compared the two. In this study, the European sea urchin, Echinus esculentus was exposed to low salinity over the short-term (11, 16, 21, 26, and 31‰ for 24 hours) and longer-term (21, 26, and 31‰ for 25 days). Over the short-term, oxygen consumption, activity coefficient and coelomic fluid osmolality were directly correlated with reduced salinity, with 100% survival at ≥21‰ and 0% at ≤16‰. Over the longer-term at 21‰ (25 days), oxygen consumption was significantly higher, feeding was significantly reduced, and activity coefficient values were significantly lower than at control salinity (31‰). At 26‰, all metrics were comparable to the control by the end of the experiment, suggesting acclimation. Furthermore, beneficial functional resistance (righting ability and metabolic capacity) to acute low salinity was observed at 26‰. Osmolality values were slightly hyperosmotic to the external seawater at all acclimation salinities, while coelomocyte composition and concentration were unaffected by chronic low salinity. Overall, E. esculentus demonstrate phenotypic plasticity that enables acclimation to reduced salinity around 26‰; however, 21‰ represents a lower acclimation threshold, likely limiting its distribution in coastal areas prone to high freshwater input

Dynamical ionization ignition of clusters in intense and short laser pulses

The electron dynamics of rare gas clusters in laser fields is investigated quantum mechanically by means of time-dependent density functional theory. The mechanism of early inner and outer ionization is revealed. The formation of an electron wave packet inside the cluster shortly after the first removal of a small amount of electron density is observed. By collisions with the cluster boundary the wave packet oscillation is driven into resonance with the laser field, hence leading to higher absorption of laser energy. Inner ionization is increased because the electric field of the bouncing electron wave packet adds up constructively to the laser field. The fastest electrons in the wave packet escape from the cluster as a whole so that outer ionization is increased as well.Comment: 8 pages, revtex4, PDF-file with high resolution figures is available from http://mitarbeiter.mbi-berlin.de/bauer/publist.html, publication no. 24. Accepted for publication in Phys. Rev.

Diel vertical migration of Arctic zooplankton during the polar night

High-latitude environments show extreme seasonal variation in physical and biological variables. The classic paradigm of Arctic marine ecosystems holds that most biological processes slow down or cease during the polar night. One key process that is generally assumed to cease during winter is diel vertical migration (DVM) of zooplankton. DVM constitutes the largest synchronized movement of biomass on the planet, and is of paramount importance for marine ecosystem function and carbon cycling. Here we present acoustic data that demonstrate a synchronized DVM behaviour of zooplankton that continues throughout the Arctic winter, in both open and ice-covered waters. We argue that even during the polar night, DVM is regulated by diel variations in solar and lunar illumination, which are at intensities far below the threshold of human perception. We also demonstrate that winter DVM is stronger in open waters compared with ice-covered waters. This suggests that the biologically mediated vertical flux of carbon will increase if there is a continued retreat of the Arctic winter sea ice cover