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Diel Vertical Migration of Arctic Zooplankton During the Polar Night

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Diel Vertical Migration of Arctic Zooplankton During the Polar Night Biol. Lett. tune their behaviour to the migration pattern of their doi:10.1098/rsbl.2008.0484 zooplankton prey (Hays 2003). Published online The absolute and relative changes in downwelling K2 K1 Marine biology irradiance (Ed, mmol photons m s at 400–700 nm) are considered the universal proximate trigger for DVM (Ringelberg 1999; Ringelberg & Van Gool 2003). Diel vertical migration of There is an apparent absence of Ed during the polar night, defined here as the seasonal period when the Sun Arctic zooplankton during is more than 128 below the horizon, which humans perceive as being continuously dark. This, combined the polar night with the strong attenuation of light by sea ice, leads to the conventional paradigm that DVM should cease Jørgen Berge1,2,*, Finlo Cottier2, Kim S. Last2, completely during winter in the Arctic marine environ- Øystein Varpe1, Eva Leu3, Janne Søreide1, 4 3 2 ment. This understanding is entirely commensurate Ketil Eiane , Stig Falk-Petersen , Kate Willis , with the low food availability in winter (Smetacek & Henrik Nyga˚rd1, Daniel Vogedes1, Colin Griffiths2, 1,5 1 Nicol 2005) and the dormant overwintering strategies Geir Johnsen , Dag Lorentzen of some zooplankton species (Fortier et al. 2001; 6 and Andrew S. Brierley Falk-Petersen et al. in press). 1University Centre in Svalbard, Pb 156, 9171 Longyearbyen, Norway Most studies of DVM in the Arctic have focused 2 The Scottish Association for Marine Science, Dunstaffnage Marine on the period of midnight sun (Fortier et al. 2001; Laboratories, Oban, Argyll PA37 1QA, UK 3Norwegian Polar Institute, 9296 Tromsø, Norway Blachowiak-Samolyk et al. 2006) or on the transition 4Bodø University College, 8049 Bodø, Norway period between midnight sun and the overt day/night 5Trondhjem biological station, Norwegian University of Science and daily cycle (Blachowiak-Samolyk et al. 2006; Cottier Technology, 7491 Trondheim, Norway et al. 2006; Falk-Petersen et al. in press). There are 6Gatty Marine Laboratory, University of St Andrews, St Andrews, Fife KY16 8LB, UK few studies of biological processes during the polar *Author for correspondence ( [email protected]). night, largely owing to the logistical difficulties of High-latitude environments show extreme seaso- sampling. One DVM study carried out in the Green- nal variation in physical and biological variables. land Sea during winter failed to detect a clear vertical The classic paradigm of Arctic marine ecosystems migration pattern during the period from November holds that most biological processes slow down or to January (Fischer & Visbeck 1993). cease during the polar night. One key process that Here we use acoustic data from two coastal is generally assumed to cease during winter is diel locations in Svalbard (Kongsfjorden and Rijpfjorden vertical migration (DVM) of zooplankton. DVM at 798 and 808 N, respectively) to test the hypothesis constitutes the largest synchronized movement of that there is no DVM behaviour during the polar biomass on the planet, and is of paramount night. Although both locations are at similar high importance for marine ecosystem function and latitudes, their oceanographic properties are represen- carbon cycling. Here we present acoustic data that demonstrate a synchronized DVM behaviour tative of the extremes found throughout the Arctic. In of zooplankton that continues throughout the combination, the results from these sites provide data Arctic winter, in both open and ice-covered that are relevant on a pan-Arctic scale (see the waters. We argue that even during the polar night, electronic supplementary material). DVM is regulated by diel variations in solar and lunar illumination, which are at intensities far below the threshold of human perception. We also 2. MATERIAL AND METHODS demonstrate that winter DVM is stronger in open Acoustic data were collected continuously at each study site using moored, upward-looking 300 kHz acoustic Doppler current profi- waters compared with ice-covered waters. This lers (ADCP). These data were analysed for temporal and spatial suggests that the biologically mediated vertical changes in the intensity of the acoustic backscatter signal to flux of carbon will increase if there is a continued determine the presence, timing and amplitude of DVM. Backscatter retreat of the Arctic winter sea ice cover. intensity from a given depth in the water is positively correlated with the biomass of zooplankton there (figure 1). Temporal Keywords: diel vertical migration; circadian; variation in echo intensity with depth is indicative of synchronized polar night; Arctic; zooplankton; solar DVM (Cottier et al. 2006). The occurrence, synchronicity and depth range of DVM signals were determined using the circadian statistical analysis program CLEAN (Rosato & Kyriacou 2006). Since migrations occur as a movement of biomass through large parts of water column, the CLEAN spectral and autocorrelation 1. INTRODUCTION analyses were applied to each depth layer independently (figure 1), Many marine predators search for their prey visually, thus enhancing the spatial and temporal resolutions with which the and their search efficiency is directly linked to ambient periodicity of these migrations were estimated (see the electronic irradiance intensity (Yo s h i d a et al. 2004). Conse- supplementary material). A sediment trap on each mooring collected samples of zooplankton, which offer insight to the likely quently, herbivorous zooplankton have evolved a pre- species composition of the migrating population (Willis et al. 2006). dator-avoidance behaviour (Hays 2003) known as diel vertical migration (DVM). Zooplankton ascend into food-rich surface waters during darkness and retreat to 3. RESULTS deeper waters during day (Fortier et al. 2001). These The output from the CLEAN analysis (figure 2) vertical migrations are integral to structuring pelagic summarizes the DVM signal. It shows 24-hour communities and food webs because pelagic predators periodicity for each depth layer for defined periods throughout the polar night. From this, it is clear that Electronic supplementary material is available at http://dx.doi.org/ zooplankton at both sites do perform DVM through 10.1098/rsbl.2008.0484 or via http://journals.royalsociety.org. most of the Arctic winter, even in those periods of the Received 24 August 2008 Accepted 30 September 2008 This journal is q 2008 The Royal Society 2 J. Berge et al. DVM during polar night (a) 0 –20 –70 –40 –80 –60 depth (m) –80 –90 –100 09 Feb 10 Feb 11 Feb 12 Feb 13 Feb 14 Feb 15 Feb 16 Feb 17 Feb dB (b) –65 –70 –75 –80 –85 backscatter (dB) –90 09 Feb 10 Feb 11 Feb 12 Feb 13 Feb 14 Feb 15 Feb 16 Feb 17 Feb (c) 0.8 0.6 0.4 0.2 spectral units 0 6121824 30 period (h) (d) 1.0 0.8 0.6 0.4 units 0.2 0 autocorrelation –0.2 12 24 36 48 60 72 84 96 period (h) Figure 1. Derivation of the autocorrelation values for the periodicity of DVM using an example from the 30 to 34 m depth interval. (a) Backscatter values in the upper 100 m in Kongsfjorden. (b) Backscatter values from 30 to 34 m for the same period as in (a). Calculation of the dominant periods and strength of the periods in the backscatter data shown in (b) using (c) CLEAN spectral analysis and (d ) autocorrelation routines in the MAZ software (Rosato & Kyriacou 2006). The spectrogram (c) shows three periodic components above the 99 per cent confidence limit (red line): 8 and 11.9 hours (peaks in the dusk/dawn ascent and descent patterns) and 24.1 hours (daily migration pattern). The correlogram (d ) reconfirms the spectral analysis result with the strongest correlations at periods of 24 hours (the 48, 72 and 96 hours peaks are harmonics and ignored). The strength of the DVM signal is represented by the height of the 24-hour peak, which in this case is 0.64 and equates to highly synchronized activity. polar night with seemingly no diel changes in Ed. the upper 80 m in Kongsfjorden during a period with Although the strongest DVM signal over the greatest no apparent light trigger. From the beginning of vertical extent was detected at both sites in October February, when the Sun rose above the horizon, the and March when the Sun was above the horizon, DVM signal was strong throughout the water column giving a distinct contrast in irradiance between day at both sites. However, in Rijpfjorden where sea ice and night, a near-continuous, albeit reduced, DVM hadformed,theDVMpatternshowedaslightly signal was detected at both sites during the polar reduced depth range and synchronicity compared night (figure 2). with Kongsfjorden. By early March, with a strong In Kongsfjorden, planktic organisms performed day–night cycle of irradiance, active DVM was occur- DVM from the middle of December until early ring in Rijpfjorden under a sea ice cover of up to 1 m January, within the period of the polar night, in a thickness ( J. Berge 2007, personal observation). depth range limited to 30–60 m. However, from early The overall acoustic backscatter signal was stronger January onwards the strength of the DVM pattern in Kongsfjorden, indicating a larger total migrating and its depth range increased in both fjords. At this biomass. Furthermore, sediment trap samples from time, a clear DVM signal was discernable throughout Kongsfjorden contained more zooplankton individuals Biol. Lett. DVM during polar night J. Berge et al. 3 (a) LD DD LD L <6h L <6h 6h<L <12h 0 Rijpfjorden sea ice –20 –40 –60 depth (m) autocorrelation value –80 1.0 –100 0.8 0.6 04 Jan 02 Mar 01 Oct 21 Oct 01 Feb 22 Feb 10 Dec 18 Mar 15 Nov (b) LD DD LD 0.4 0 L <6h L <6h 6h<L <12h Kongsfjorden 0.2 increasing rhythmicity –20 0 –40 –60 depth (m) –80 –100 08 Jan 01 Oct 25 Oct 01 Feb 18 Feb 27 Feb 14 Dec 18 Mar 19 Nov Figure 2.
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