Abstract
Recent studies have shown that the biological activity during the Arctic polar night is higher than previously thought. Zooplankton perform diel vertical migration during the dark period/winter, with the calanoid copepods Calanus spp. being one of the main taxa assumed to contribute to the observed diel vertical migration. We investigated the sensitivity of field-collected Calanus spp. to irradiance by keeping individuals in an aquarium and exposing them to gradually increasing irradiance in white, blue, green, and red wavebands, recording their phototactic response with a near-infrared-sensitive video camera. Experiments were performed with the two oldest copepodite stages as well as adult males and females. The copepods were negatively phototactic, and the lowest irradiance eliciting a significant phototactic response was of the order of 10−8–10−6 μmol photons m−2 s−1 for white, green, and blue wavebands, whereas the comparative irradiance for red wavebands was up to three orders of magnitudes higher. The different copepod developmental stages displayed different sensitivities to irradiance. During the darkest part of the polar night, the lowest irradiance for significant response corresponded to 0.0005–0.5 % of the ambient surface irradiance, depending on light source. Accordingly, Calanus spp. may respond to irradiance from the night sky down to 70–80 m, moonlight to 120–170 m, and aurora borealis down to 80–120 m depth. The high sensitivity to blue and green light may explain the Calanus’ ability to perform diel vertical migration during the polar night when intensity and diurnal variation of ambient irradiance is low.
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References
Aarseth KA, Schram TA (1999) Wavelength-specific behaviour in Lepeophtheirus salmonis and Calanus finmarchicus to ultraviolet and visible light in laboratory experiments (Crustacea: Copepoda). Mar Ecol Prog Ser 186:211–217
Arnkværn G, Daase M, Eiane K (2005) Dynamics of coexisting Calanus finmarchicus, Calanus glacialis and Calanus hyperboreus populations in a high-Arctic fjord. Polar Biol 28:528–538
Auel H, Werner I (2003) Feeding, respiration and life history of the hyperiid amphipod Themisto libellula in the Arctic marginal ice zone of the Greenland Sea. J Exp Mar Biol Ecol 296:183–197
Baker DJ, Romick GJ (1976) The rayleigh: interpretation of the unit in terms of column emission rate or apparent radiance expressed in SI units. Appl Opt 15:1966–1968
Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package version 0.999375-42. http://CRAN.R-project.org/package=lme4
Baumgartner MF, Mate BR (2003) Summertime foraging ecology of North Atlantic right whales. Mar Ecol Prog Ser 264:123–135
Baumgartner MF, Cole TVN, Campbell RG, Teegarden GJ, Durbin EG (2003) Associations between North Atlantic right whales and their prey, Calanus finmarchicus, over diel and tidal time scales. Mar Ecol Prog Ser 264:155–166
Baumgartner MF, Lysiak NSJ, Schuman C, Urban-Rich J, Wenzel FW (2011) Diel vertical migration behavior of Calanus finmarchicus and its influence on right and sei whale occurrence. Mar Ecol Prog Ser 423:167–184
Berge J, Cottier F, Last KS, Varpe Ø, Leu E, Søreide J, Eiane K, Falk-Petersen S, Willis K, Nygård H, Vogedes D, Griffiths C, Johnsen G, Lorentzen D, Brierley AS (2009) Diel vertical migration of Arctic zooplankton during the polar night. Biol Lett 5:69–72
Berge J, Båtnes AS, Johnsen G, Blackwell SM, Moline MA (2012) Bioluminescence in the high Arctic during the polar night. Mar Biol 159:231–237
Bergvik M, Leiknes Ø, Altin D, Dahl KR, Olsen Y (2012) Dynamics of the lipid content and biomass of Calanus finmarchicus (copepodite V) in a Norwegian fjord. Lipids 47:881–895
Blachowiak-Samolyk K, Søreide JE, Kwasniewski S, Sundfjord A, Hop H, Falk-Petersen S, Hegseth EN (2008) Hydrodynamic control of mesozooplankton abundance and biomass in northern Svalbard waters (79-81°N). Deep-Sea Res II 55:2210–2224
Clarke GL (1971) Light conditions in the sea in relation to the diurnal vertical migration of animals. In: Farquhar GB (ed) Proceedings of the International Symposium on Biological Sound Scattering in Ocean. Maury Center for Ocean Science, Washington, pp 41–50
Cohen JH, Forward RB Jr (2002) Spectral sensitivity of vertically migrating marine copepods. Biol Bull (Woods Hole) 203:307–314
Cohen JH, Forward RB Jr (2005) Diel vertical migration of the marine copepod Calanopia americana. II. Proximate role of exogenous light cues and endogenous rhythms. Mar Biol 147:399–410
Cohen JH, Forward RB Jr (2009) Zooplankton diel vertical migration—a review of proximate control. In: Gibson RN, Atkinson RJA, Gordon JDM (eds) Oceanography and marine biology: an annual review, vol 47. CRC Press, Boca Raton, pp 77–109
Conover RJ (1988) Comparative life histories in the genera Calanus and Neocalanus in high latitudes of the northern hemisphere. Hydrobiol 167(168):127–142
Cottier FR, Tarling GA, Wold A, Falk-Petersen S (2006) Unsynchronized and synchronized vertical migration of zooplankton in a high arctic fjord. Limnol Oceanogr 51:2586–2599
Daase M, Eiane K, Aksnes DL, Vogedes D (2008) Vertical distribution of Calanus spp. and Metridia longa at four Arctic locations. Mar Biol Res 4:193–207
Dale T, Kaartvedt S (2000) Diel patterns in stage-specific vertical migration of Calanus finmarchicus in habitats with midnight sun. ICES J Mar Sci 57:1800–1818
Dupont N, Aksnes DL (2012) Effects of bottom depth and water clarity on the vertical distribution of Calanus spp. J Plankton Res 34:263–266
Falk-Petersen S, Hopkins CCE, Sargent JR (1990) Trophic relationships in the pelagic, Arctic food web. In: Barnes M, Gibson RN (eds) Trophic relationships in the marine environment. Aberdeen University Press, Aberdeen, pp 315–333
Falk-Petersen S, Leu E, Berge J, Kwaśniewski S, Nygård H, Røstad A, Keskinen E, Thormar J, von Quillfeldt C, Wold A, Gulliksen B (2008) Vertical migration in high Arctic waters during Autumn 2004. Deep Sea Res II 55:2275–2284
Falk-Petersen S, Mayzaud P, Kattner G, Sargent JR (2009) Lipids and life strategy of Arctic Calanus. Mar Biol Res 5:18–39
Fort J, Cherel Y, Harding AMA, Egevang E, Steen H, Kuntz G (2010) The feeding ecology of little auks raises questions about winter zooplankton stocks in North Atlantic surface waters. Biol Lett 6:682–684
Fortier M, Fortier L, Hattori H, Saito H, Legendre L (2001) Visual predators and the diel vertical migration of copepods under Arctic sea ice during the midnight sun. J Plankton Res 23:1263–1278
Forward RB (1988) Diel vertical migration: zooplankton photobiology and behaviour. Oceanogr Mar Biol Annu Rev 26:361–393
Frost BW (1988) Variability and possible significance of diel vertical migration in Calanus pacificus, a planktonic marine copepod. Bull Mar Sci 43:675–694
Gabrielsen TM, Merkel B, Søreide JE, Johansson-Karlsson E, Bailey A, Vogedes D, Nygård H, Varpe Ø, Berge J (2012) Potential misidentifications of two climate indicator species of the marine arctic ecosystem: Calanus glacialis and C. finmarchicus. Polar Biol 35:1621–1628
Hassel A (1986) Seasonal changes in zooplankton composition in the Barents Sea, with special attention to Calanus spp. (Copepoda). J Plankton Res 8:329–339
Hays GC (2003) A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Hydrobiol 503:163–170
Hays GC, Kennedy H, Frost BW (2001) Individual variability in diel vertical migration of a marine copepod: why some individuals remain at depth when others migrate. Limnol Oceanogr 46:2050–2054
Hirche H-J (1991) Distribution of dominant calanoid copepod species in the Greenland Sea during late fall. Polar Biol 11:351–362
Hop H, Falk-Petersen S, Svendsen H, Kwasniewski S, Pavlov V, Pavlova O, Søreide JE (2006) Physical and biological characteristics of the pelagic system across Fram Strait to Kongsfjorden. Prog Oceanogr 71:182–231
Hovland EK, Hancke K, Alver MO, Drinkwater K, Høkedal J, Johnsen G, Moline M, Sakshaug E (2012) Optical impact of an Emiliania huxleyi bloom in the frontal region of the Barents Sea. J Mar Syst. doi:10.1016/j.jmarsys.2012.07.002
Huntley M, Brooks ER (1982) Effects of age and food availability on diel vertical migration of Calanus pacificus. Mar Biol 71:23–31
Irigoien X, Obermuller B, Head RN, Harris RP, Rey C, Hansen BW, Hygum BH, Heath MR, Durbin EG (2000) The effect of food on the determination of sex ratio in Calanus spp.: evidence from experimental studies and field data. ICES J Mar Sci 57:1752–1763
Jensen HW, Durand F, Stark M, Premoze S, Dorsey J, Shirley P (2001) A physically-based night sky model. Proc SIGGRAPH. doi:10.1145/383259.383306
Jerlov NG (1968) Optical oceanography. Elsevier, Amsterdam
Johnsen G, Volent Z, Sakshaug E, Sigernes F, Pettersson LH (2009) Remote sensing in the Barens Sea. In: Sakshaug E, Johnsen G, Kovacs K (eds) Ecosystem Barents Sea. Tapir Academic Press, Trondheim, pp 139–168
Karnovsky NJ, Kwaśniewski S, Weşławski JM, Walkusz W, Beszczynska-Möller A (2003) Foraging behavior of little auks in a heterogeneous environment. Mar Ecol Prog Ser 253:289–303
Kiørboe T, Bagøien E (2005) Motility patterns and mate encounter rates in planktonic copepods. Limnol Oceanogr 50:1999–2007
Kwasniewski S, Hop H, Falk-Petersen S, Pedersen G (2003) Distribution of Calanus species in Kongsfjorden, a glacial fjord in Svalbard. J Plankton Res 25:1–20
Lampert W (1989) The adaptive significance of diel vertical migration of zooplankton. Funct Ecol 3:21–27
Lindeque PK, Harris RP, Jones MB, Smerdon GR (2004) Distribution of Calanus spp as determined using a genetic identification system. Sci Mar 68:121–128
Miller CB, Cowles TJ, Wiebe PH, Copley NJ, Grigg H (1991) Phenology in Calanus finmarchicus; hypotheses about control mechanisms. Mar Ecol Prog Ser 72:79–91
Müller A, Wuchterl G, Sarazin M (2011) Measuring the night sky brightness with the lightmeter. RevMexAA (Serie de Conferencias) 41:46–49
Mumm N, Auel H, Hanssen H, Hagen W, Richter C, Hirche HJ (1998) Breaking the ice: large-scale distribution of mesozooplankton after a decade of Arctic and transpolar cruises. Polar Biol 20:189–197
Myrabø HK (1985) Nocturnal ground irradiance at high latitudes. Appl Optics 24:3908–3913
Nicholls AG (1933) On the biology of Calanus finmarchicus. III. Vertical distribution and diurnal migration in the Clyde-Sea area. J Mar Biol Assoc UK 19:139–164
Parent GJ, Plourde S, Turgeon J (2011) Overlapping size ranges of Calanus spp. off the Canadian Arctic and Atlantic coasts: impact on species’ abundances. J Plankton Res 33:1654–1665
Parent GJ, Plourde S, Turgeon J (2012) Natural hybridization between Calanus finmarchicus and C. glacialis (Copepoda) in the Arctic and Northwest Atlantic. Limnol Oceanogr 57:1057–1066
Pulkkinen TI, Tanskanen EI, Viljanen A, Partamies N, Kauristie K (2011) Auroral electrojets during deep solar minimum at the end of solar cycle 23. J Geophys Res. doi:10.1029/2010JA016098
R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0
Rabindranath A, Daase M, Falk-Petersen S, Wold A, Wallace MI, Berge J, Brierley AS (2011) Seasonal and diel vertical migration of zooplankton in the High Arctic during the autumn midnight sun of 2008. Mar Biodivers 41:365–382
Rasband WS (1997–2012) ImageJ, U.S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/
Ringelberg J (1995) Changes in light-intensity and diel vertical migration—a comparison of marine and freshwater environments. J Mar Biol Assoc UK 75:15–25
Ringelberg J (1999) The photobehaviour of Daphnia spp. as a model to explain diel vertical migration in zooplankton. Biol Rev Cambridge Philos Soc 74:397–423
Ringelberg J, Van Gool E (2003) On the combined analysis of proximate and ultimate aspects in diel vertical migration (DVM) research. Hydrobiol 491:85–90
Sakshaug E, Johnsen G, Zsolt V (2009) Light. In: Sakshaug E, Johnsen G, Kovacs K (eds) Ecosystem Barents Sea. Tapir Academic Press, Trondheim, pp 117–138
Sato M, Sasaki H, Fukuchi M (2002) Stable isotopic compositions of overwintering copepods in the arctic and subarctic waters and implications to the feeding history. J Mar Syst 38:165–174
Simmons DAR, Sigernes F, Henriksen K (1996) Weather, twilight, and auroral observing from Spitsbergen in the polar winter. Polar Rec 32:217–228
Søreide JE, Falk-Petersen S, Hegseth EN, Hop H, Carroll ML, Hobson KA, Blachowiak-Samolyk K (2008) Seasonal feeding strategies of Calanus in the high-Arctic Svalbard region. Deep-Sea Res II 55:2225–2244
Stearns DE, Forward RB (1984) Photosensitivity of the calanoid copepod Acartia tonsa. Mar Biol 82:85–89
Tande KS (1982) Ecological investigations on the zooplankton community in Balsfjorden, northern Norway: generation cycles, and variations in body weight and body content of carbon and nitrogen related to overwintering and reproduction in the copepod Calanus finmarchicus (Gunnerus). J Exp Mar Biol Ecol 62:129–142
Tande KS (1988) An evaluation of factors affecting vertical distribution among recruits of Calanus finmarchicus in three adjacent high-latitude localities. Hydrobiol 167–168:115–126
Unstad KH, Tande KS (1991) Depth distribution of Calanus finmarchicus and Calanus glacialis in relation to environmental conditions in the Barents Sea. Polar Res 10:409–420
Vadstein (2009) Interactions the planktonic food web. In: Sakshaug E, Johnsen G, Kovacs KM (eds) Ecosystem Barents Sea. Tapir Academic Press, Trondheim, pp 251–266
Wallace MI, Cottier FR, Berge J, Tarling GA, Griffiths C, Brierley AS (2010) Comparison of zooplankton vertical migration in an ice-free and a seasonally ice-covered Arctic fjord: an insight into the influence of sea ice cover on zooplankton behavior. Limnol Oceanogr 55:831–845
Webster CN, Varpe Ø, Falk-Petersen S, Berge J, Stübner E, Brierley AS (in press) Moonlit swimming: vertical distributions of macrozooplankton and nekton during the polar night. Polar Biol
Wold A, Norrbin F (2004) Vertical migration as a response to UVR stress in Calanus finmarchicus females and nauplii. Polar Res 23:27–34
Yamagutchi A, Ikeda T, Watanabe Y, Ishizaka J (2004) Vertical distribution patterns of pelagic copepods as viewed from the predation pressure hypothesis. Zool Stud 43:475–485
Acknowledgements
Funding for the Ph.D. Project of A. S. Båtnes was provided by the Faculty of Natural Sciences and Technology (SO funding), NTNU, and the field work was funded by the Arctic Field Grant (Svalbard Science Forum, Norwegian Polar institute). The Ph.D. Project of C. Miljeteig was funded by VISTA—a basic research programme funded by Statoil, conducted in close collaboration with The Norwegian Academy of Science and Letters (Project No. 6156). J. Berge is supported by the Norwegian Research Council project Circa (Project No. 214271). M. Greenacre’s research is partially supported by the BBVA Foundation in Madrid and grant MTM2012-37195 of the Spanish Ministry of Education and Competitiveness.
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Båtnes, A.S., Miljeteig, C., Berge, J. et al. Quantifying the light sensitivity of Calanus spp. during the polar night: potential for orchestrated migrations conducted by ambient light from the sun, moon, or aurora borealis?. Polar Biol 38, 51–65 (2015). https://doi.org/10.1007/s00300-013-1415-4
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DOI: https://doi.org/10.1007/s00300-013-1415-4