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Polar Biology

, Volume 38, Issue 1, pp 51–65 | Cite as

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?

  • Anna S. Båtnes
  • Cecilie Miljeteig
  • Jørgen Berge
  • Michael Greenacre
  • Geir Johnsen
Original Paper

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.

Keywords

Phototaxis Light response Spectral sensitivity Copepods Arctic 

Notes

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.

Supplementary material

300_2013_1415_MOESM1_ESM.docx (3.4 mb)
Supplementary material 1 (DOCX 3523 kb)
300_2013_1415_MOESM2_ESM.tif (3.1 mb)
Supplementary material 2 (TIFF 3174 kb)

References

  1. 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 186:211–217CrossRefGoogle Scholar
  2. 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 28:528–538CrossRefGoogle Scholar
  3. 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 296:183–197CrossRefGoogle Scholar
  4. 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 15:1966–1968PubMedCrossRefGoogle Scholar
  5. 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
  6. Baumgartner MF, Mate BR (2003) Summertime foraging ecology of North Atlantic right whales. Mar Ecol Prog Ser 264:123–135CrossRefGoogle Scholar
  7. 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 264:155–166CrossRefGoogle Scholar
  8. 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 423:167–184CrossRefGoogle Scholar
  9. 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 5:69–72PubMedCentralPubMedCrossRefGoogle Scholar
  10. Berge J, Båtnes AS, Johnsen G, Blackwell SM, Moline MA (2012) Bioluminescence in the high Arctic during the polar night. Mar Biol 159:231–237PubMedCentralPubMedCrossRefGoogle Scholar
  11. 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 47:881–895PubMedCrossRefGoogle Scholar
  12. 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 55:2210–2224CrossRefGoogle Scholar
  13. 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 41–50Google Scholar
  14. Cohen JH, Forward RB Jr (2002) Spectral sensitivity of vertically migrating marine copepods. Biol Bull (Woods Hole) 203:307–314CrossRefGoogle Scholar
  15. 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 147:399–410CrossRefGoogle Scholar
  16. 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 77–109CrossRefGoogle Scholar
  17. Conover RJ (1988) Comparative life histories in the genera Calanus and Neocalanus in high latitudes of the northern hemisphere. Hydrobiol 167(168):127–142CrossRefGoogle Scholar
  18. Cottier FR, Tarling GA, Wold A, Falk-Petersen S (2006) Unsynchronized and synchronized vertical migration of zooplankton in a high arctic fjord. Limnol Oceanogr 51:2586–2599CrossRefGoogle Scholar
  19. Daase M, Eiane K, Aksnes DL, Vogedes D (2008) Vertical distribution of Calanus spp. and Metridia longa at four Arctic locations. Mar Biol Res 4:193–207CrossRefGoogle Scholar
  20. Dale T, Kaartvedt S (2000) Diel patterns in stage-specific vertical migration of Calanus finmarchicus in habitats with midnight sun. ICES J Mar Sci 57:1800–1818CrossRefGoogle Scholar
  21. Dupont N, Aksnes DL (2012) Effects of bottom depth and water clarity on the vertical distribution of Calanus spp. J Plankton Res 34:263–266CrossRefGoogle Scholar
  22. 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 315–333Google Scholar
  23. 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 55:2275–2284CrossRefGoogle Scholar
  24. Falk-Petersen S, Mayzaud P, Kattner G, Sargent JR (2009) Lipids and life strategy of Arctic Calanus. Mar Biol Res 5:18–39CrossRefGoogle Scholar
  25. 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 6:682–684PubMedCentralPubMedCrossRefGoogle Scholar
  26. 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 23:1263–1278CrossRefGoogle Scholar
  27. Forward RB (1988) Diel vertical migration: zooplankton photobiology and behaviour. Oceanogr Mar Biol Annu Rev 26:361–393Google Scholar
  28. Frost BW (1988) Variability and possible significance of diel vertical migration in Calanus pacificus, a planktonic marine copepod. Bull Mar Sci 43:675–694Google Scholar
  29. 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 35:1621–1628CrossRefGoogle Scholar
  30. Hassel A (1986) Seasonal changes in zooplankton composition in the Barents Sea, with special attention to Calanus spp. (Copepoda). J Plankton Res 8:329–339CrossRefGoogle Scholar
  31. Hays GC (2003) A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Hydrobiol 503:163–170CrossRefGoogle Scholar
  32. 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 46:2050–2054CrossRefGoogle Scholar
  33. Hirche H-J (1991) Distribution of dominant calanoid copepod species in the Greenland Sea during late fall. Polar Biol 11:351–362CrossRefGoogle Scholar
  34. 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 71:182–231CrossRefGoogle Scholar
  35. 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 Google Scholar
  36. Huntley M, Brooks ER (1982) Effects of age and food availability on diel vertical migration of Calanus pacificus. Mar Biol 71:23–31CrossRefGoogle Scholar
  37. 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 57:1752–1763CrossRefGoogle Scholar
  38. 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
  39. Jerlov NG (1968) Optical oceanography. Elsevier, AmsterdamGoogle Scholar
  40. 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 139–168Google Scholar
  41. 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 253:289–303CrossRefGoogle Scholar
  42. Kiørboe T, Bagøien E (2005) Motility patterns and mate encounter rates in planktonic copepods. Limnol Oceanogr 50:1999–2007CrossRefGoogle Scholar
  43. Kwasniewski S, Hop H, Falk-Petersen S, Pedersen G (2003) Distribution of Calanus species in Kongsfjorden, a glacial fjord in Svalbard. J Plankton Res 25:1–20CrossRefGoogle Scholar
  44. Lampert W (1989) The adaptive significance of diel vertical migration of zooplankton. Funct Ecol 3:21–27CrossRefGoogle Scholar
  45. Lindeque PK, Harris RP, Jones MB, Smerdon GR (2004) Distribution of Calanus spp as determined using a genetic identification system. Sci Mar 68:121–128CrossRefGoogle Scholar
  46. Miller CB, Cowles TJ, Wiebe PH, Copley NJ, Grigg H (1991) Phenology in Calanus finmarchicus; hypotheses about control mechanisms. Mar Ecol Prog Ser 72:79–91CrossRefGoogle Scholar
  47. Müller A, Wuchterl G, Sarazin M (2011) Measuring the night sky brightness with the lightmeter. RevMexAA (Serie de Conferencias) 41:46–49Google Scholar
  48. 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 20:189–197CrossRefGoogle Scholar
  49. Myrabø HK (1985) Nocturnal ground irradiance at high latitudes. Appl Optics 24:3908–3913CrossRefGoogle Scholar
  50. 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 19:139–164CrossRefGoogle Scholar
  51. 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 33:1654–1665CrossRefGoogle Scholar
  52. Parent GJ, Plourde S, Turgeon J (2012) Natural hybridization between Calanus finmarchicus and C. glacialis (Copepoda) in the Arctic and Northwest Atlantic. Limnol Oceanogr 57:1057–1066CrossRefGoogle Scholar
  53. 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 Google Scholar
  54. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0Google Scholar
  55. 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 41:365–382CrossRefGoogle Scholar
  56. Rasband WS (1997–2012) ImageJ, U.S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/
  57. Ringelberg J (1995) Changes in light-intensity and diel vertical migration—a comparison of marine and freshwater environments. J Mar Biol Assoc UK 75:15–25CrossRefGoogle Scholar
  58. Ringelberg J (1999) The photobehaviour of Daphnia spp. as a model to explain diel vertical migration in zooplankton. Biol Rev Cambridge Philos Soc 74:397–423CrossRefGoogle Scholar
  59. Ringelberg J, Van Gool E (2003) On the combined analysis of proximate and ultimate aspects in diel vertical migration (DVM) research. Hydrobiol 491:85–90CrossRefGoogle Scholar
  60. Sakshaug E, Johnsen G, Zsolt V (2009) Light. In: Sakshaug E, Johnsen G, Kovacs K (eds) Ecosystem Barents Sea. Tapir Academic Press, Trondheim, pp 117–138Google Scholar
  61. 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 38:165–174CrossRefGoogle Scholar
  62. Simmons DAR, Sigernes F, Henriksen K (1996) Weather, twilight, and auroral observing from Spitsbergen in the polar winter. Polar Rec 32:217–228CrossRefGoogle Scholar
  63. 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 55:2225–2244CrossRefGoogle Scholar
  64. Stearns DE, Forward RB (1984) Photosensitivity of the calanoid copepod Acartia tonsa. Mar Biol 82:85–89CrossRefGoogle Scholar
  65. 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 62:129–142CrossRefGoogle Scholar
  66. Tande KS (1988) An evaluation of factors affecting vertical distribution among recruits of Calanus finmarchicus in three adjacent high-latitude localities. Hydrobiol 167–168:115–126CrossRefGoogle Scholar
  67. Unstad KH, Tande KS (1991) Depth distribution of Calanus finmarchicus and Calanus glacialis in relation to environmental conditions in the Barents Sea. Polar Res 10:409–420CrossRefGoogle Scholar
  68. Vadstein (2009) Interactions the planktonic food web. In: Sakshaug E, Johnsen G, Kovacs KM (eds) Ecosystem Barents Sea. Tapir Academic Press, Trondheim, pp 251–266Google Scholar
  69. 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 55:831–845CrossRefGoogle Scholar
  70. 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 BiolGoogle Scholar
  71. Wold A, Norrbin F (2004) Vertical migration as a response to UVR stress in Calanus finmarchicus females and nauplii. Polar Res 23:27–34CrossRefGoogle Scholar
  72. Yamagutchi A, Ikeda T, Watanabe Y, Ishizaka J (2004) Vertical distribution patterns of pelagic copepods as viewed from the predation pressure hypothesis. Zool Stud 43:475–485Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Anna S. Båtnes
    • 1
    • 2
  • Cecilie Miljeteig
    • 1
  • Jørgen Berge
    • 3
    • 2
  • Michael Greenacre
    • 3
    • 4
  • Geir Johnsen
    • 1
    • 2
  1. 1.Department of BiologyNorwegian University of Science and TechnologyTrondheimNorway
  2. 2.The University Centre in SvalbardLongyearbyenNorway
  3. 3.Faculty of Biosciences, Fisheries and EconomicsThe Arctic University of NorwayTromsøNorway
  4. 4.Department of Economics and Business, Barcelona Graduate School of EconomicsUniversitat Pompeu FabraBarcelonaSpain

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