Polar Biology

, Volume 38, Issue 7, pp 1025–1033 | Cite as

Thermal response of ingestion and egestion rates in the Arctic copepod Calanus glacialis and possible metabolic consequences in a warming ocean

  • Ulrike Grote
  • Anna Pasternak
  • Elena Arashkevich
  • Elisabeth Halvorsen
  • Anastasia Nikishina
Original Paper

Abstract

Climate change is particularly rapid in the Arctic, where water temperatures are predicted to increase substantially with implications for Arctic marine organisms, especially ectotherms such as the calanoid copepod Calanus glacialis, a key herbivore in the Arctic marine ecosystem. Feeding depends on temperature, and recent studies indicate different thermal responses in ingestion and respiration implying a possible metabolic mismatch with increasing temperatures. We investigated the thermal response of ingestion and faecal pellet production as an indicator of egestion of the Arctic copepod C. glacialis in incubation experiments at five temperatures ranging from 0 to 10 °C and compared the obtained data with published results on temperature dependence of respiration. Copepods were fed ad libitum with the diatom Thalassiosira gravida, and algae concentration was assessed prior and after 4 h feeding experiments. Egested faecal pellets were collected and counted. Ingestion and faecal pellet production rates increased linearly (Q10 coefficient ~1.4–1.7 and ~1.8–4.1, respectively). No pronounced effect of feeding history (fed vs. starved for 3 days prior to experiment) was found, but responses in both rates were generally less dependent on temperature in the pre-starved experiment. Q10 values for ingestion rates were lower than Q10 values for published respiration rates (~1.8–4.6), indicating that metabolic losses increase stronger with increasing temperature than metabolic gains by ingestion. A persistent imbalance between metabolic losses and energy uptake could lead to reduced fitness for C.glacialis, thereby affecting the population dynamics and distribution of this important species in the Arctic.

Keywords

Feeding Temperature Climate change Calanoid copepods Ecophysiology 

References

  1. ACIA (2004) Impacts of a warming Arctic: Arctic climate impact assessment. Cambridge University Press, 1042 pGoogle Scholar
  2. Alcaraz M, Felipe J, Grote U, Arashkevich E, Nikishina A (2014) Life in a warming ocean: thermal thresholds and metabolic balance of arctic zooplankton. J Plankton Res 36:3–10. doi:10.1093/plankt/fbt111 CrossRefGoogle Scholar
  3. Almeda R, Alcaraz M, Calbet A, Saiz E (2011) Metabolic rates and carbon budget of early developmental stages of the marine cyclopoid copepod Oithona davisae. Limnol Oceanogr 56:403–414. doi:10.4319/lo.2011.56.1.0403 CrossRefGoogle Scholar
  4. Angilletta MJ, Huey RB, Frazier MR (2010) Thermodynamic effects on organismal performance: Is hotter better? Physiol Biochem Zool 83:197–206. doi:10.1086/648567 PubMedCrossRefGoogle Scholar
  5. 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. doi:10.1007/s00300-005-0715-8 CrossRefGoogle Scholar
  6. Båmstedt U (1984) Diel variations in the nutritional physiology of Calanus glacialis from Lat 78 N in the summer. Mar Biol 79:257–267. doi:10.1007/bf00393257 CrossRefGoogle Scholar
  7. Båmstedt U (1988) Ecological significance of individual variability in copepod bioenergetics. Hydrobiologia 167:43–59. doi:10.1007/bf00026293 CrossRefGoogle Scholar
  8. Båmstedt U, Eilertsen HC, Tande KS, Slagstad D, Skjoldal HR (1991) Copepod grazing and its potential impact on the phytoplankton development in the Barents Sea. Polar Res 10:339–353. doi:10.1111/j.1751-8369.1991.tb00658.x CrossRefGoogle Scholar
  9. Båmstedt U, Gifford DJ, Irigoien X, Atkinson A, Roman M (2000) 8-Feeding. In: Harris R, Wiebe P, Lenz J, Skjoldal HR, Huntley M (eds) ICES zooplankton methodology manual. Academic Press, London, pp 297–399. doi:10.1016/B978-012327645-2/50009-8 CrossRefGoogle Scholar
  10. Barquero S, Cabal JA, Anadon R, Fernandez E, Varela M, Bode A (1998) Ingestion rates of phytoplankton by copepod size fractions on a bloom associated with an off-shelf front off NW Spain. J Plankton Res 20:957–972. doi:10.1093/plankt/20.5.957 CrossRefGoogle Scholar
  11. Bautista B, Harris RP (1992) Copepod gut contents, ingestion rates and grazing impact on phytoplankton in relation to size structure of zooplankton and phytoplankton during a spring bloom. Mar Ecol Prog Ser 82:41–50. doi:10.3354/meps082041 CrossRefGoogle Scholar
  12. Carstensen J, Weydmann A, Olszewska A, Kwasniewski S (2012) Effects of environmental conditions on the biomass of Calanus spp. in the Nordic Seas. J Plankton Res 34:951–966. doi:10.1093/plankt/fbs059 CrossRefGoogle Scholar
  13. Checkley DM (1980) The egg production of a marine planktonic copepdo in relation to its fod supply—laboratory studies. Limnol Oceanogr 25:430–446CrossRefGoogle Scholar
  14. Conover RJ (1988) Comparative life histories in the genera Calanus and Neocalanus in high latitudes of the northern hemisphere. Hydrobiologia 167:127–142. doi:10.1007/bf00026299 CrossRefGoogle Scholar
  15. Daase M, Eiane K (2007) Mesozooplankton distribution in northern Svalbard waters in relation to hydrography. Polar Biol 30:969–981. doi:10.1007/s00300-007-0255-5 CrossRefGoogle Scholar
  16. Degerlund M, Eilertsen HC (2010) Main species characteristics of phytoplankton spring blooms in NE Atlantic and Arctic Waters (68–80 degrees N). Estuaries Coasts 33:242–269. doi:10.1007/s12237-009-9167-7 CrossRefGoogle Scholar
  17. Dell AI, Pawar S, Savage VM (2011) Systematic variation in the temperature dependence of physiological and ecological traits. Proc Natl Acad Sci USA 108:10591–10596. doi:10.1073/pnas.1015178108 PubMedCentralPubMedCrossRefGoogle Scholar
  18. Donelson JM, Munday PL, McCormick MI, Pankhurst NW, Pankhurst PM (2010) Effects of elevated water temperature and food availability on the reproductive performance of a coral reef fish. Mar Ecol Prog Ser 401:233–243. doi:10.3354/meps08366 CrossRefGoogle Scholar
  19. Falk-Petersen S, Mayzaud P, Kattner G, Sargent JR (2009) Lipids and life strategy of Arctic Calanus. Mar Biol Res 5:18–39. doi:10.1080/17451000802512267 CrossRefGoogle Scholar
  20. Gabrielsen TM et al (2012) Potential misidentifications of two climate indicator species of the marine arctic ecosystem: Calanus glacialis and C. finmarchicus. Polar Biol 35:1621–1628. doi:10.1007/s00300-012-1202-7 CrossRefGoogle Scholar
  21. Hansen B, Berggreen UC, Tande KS, Eilertsen HC (1990) Post-bloom grazing by Calanus glacialis, C. finmarchicus and C. hyperboreus in the region of the Polar Front, Barents Sea. Mar Biol 104:5–14. doi:10.1007/bf01313151 CrossRefGoogle Scholar
  22. Hassett RP, Landry MR (1983) Effects of food-level acclimation on digestive enzyme activities and feeding behavior of Calanus pacificus. Mar Biol 75:47–55. doi:10.1007/bf00392629 CrossRefGoogle Scholar
  23. Hassett RP, Landry MR (1990) Effects of diet and starvation on digestive enzyme activity and feeding behavior of the marine copepod Calanus pacificus. J Plankton Res 12:991–1010. doi:10.1093/plankt/12.5.991 CrossRefGoogle Scholar
  24. Hirche H-J (1987) Temperature and plankton. 2. Effects on respiration and swimming activity in copepods from the greenland sea. Mar Biol 94:347–356. doi:10.1007/bf00428240 CrossRefGoogle Scholar
  25. Hirche HJ (1996) The reproductive biology of the marine copepod, Calanus finmarchicus—a review. Ophelia 44:111–128CrossRefGoogle Scholar
  26. Ikeda T, Skjoldal HR (1989) Metabolism and elemental composition of zooplankton from the Barents Sea during early Arctic summer. Mar Biol 100:173–183. doi:10.1007/bf00391956 CrossRefGoogle Scholar
  27. IPCC (2007) Climate Change 2007: The physical science basis. Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University PressGoogle Scholar
  28. IPCC (2013) Climate Change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK and New York, NY, USAGoogle Scholar
  29. Jaschnov WA (1970) Distribution of Calanus species in the seas of the northern hemisphere. Internationale Revue der gesamten Hydrobiologie und Hydrographie 55:197–212. doi:10.1002/iroh.19700550203 CrossRefGoogle Scholar
  30. Kjellerup S, Dunweber M, Swalethorp R, Nielsen TG, Møller EF, Markager S, Hansen BW (2012) Effects of a future warmer ocean on the coexisting copepods Calanus finmarchicus and C. glacialis in Disko Bay, western Greenland. Mar Ecol Prog Ser 447:87–108. doi:10.3354/meps09551 CrossRefGoogle Scholar
  31. Kordas RL, Harley CDG, O’Connor MI (2011) Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. J Exp Mar Biol Ecol 400:218–226. doi:10.1016/j.jembe.2011.02.029 CrossRefGoogle Scholar
  32. Kosobokova KN (1998) New data on the life cycle of Calanus glacialis in the White Sea (based on the seasonal observations of the development of its genital system). Okeanologiya 38:387–396Google Scholar
  33. Kosobokova KN (1999) The reproductive cycle and life history of the Arctic copepod Calanus glacialis in the White Sea. Polar Biol 22:254–263. doi:10.1007/s003000050418 CrossRefGoogle Scholar
  34. Lemoine NP, Burkepile DE (2012) Temperature-induced mismatches between consumption and metabolism reduce consumer fitness. Ecology 93:2483–2489PubMedCrossRefGoogle Scholar
  35. Lind S, Ingvaldsen RB (2012) Variability and impacts of Atlantic Water entering the Barents Sea from the north. Deep Sea Res Part I Oceanogr Res Pap 62:70–88. doi:10.1016/j.dsr.2011.12.007 CrossRefGoogle Scholar
  36. Møller EF, Maar M, Jónasdóttir SH, Nielsen TG, Tönnesson K (2012) The effect of changes in temperature and food on the development of Calanus finmarchicus and Calanus helgolandicus populations. Limnol Oceanogr 57:211–220. doi:10.4319/lo.2012.57.1.0211 CrossRefGoogle Scholar
  37. Morozov A, Pasternak AF, Arashkevich EG (2013) Revisiting the role of individual variability in population persistence and stability. PLoS One 8:e70576. doi:10.1371/journal.pone.0070576 PubMedCentralPubMedCrossRefGoogle Scholar
  38. 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. doi:10.1007/s003000050295 CrossRefGoogle Scholar
  39. Niehoff B, Hirche HJ (2005) Reproduction of Calanus glacialis in the Lurefjord (western Norway): indication for temperature-induced female dormancy. Mar Ecol Prog Ser 285:107–115. doi:10.3354/meps285107 CrossRefGoogle Scholar
  40. Pasternak A, Riser CW, Arashkevich E, Rat’kova T, Wassmann P (2002) Calanus spp. grazing affects egg production and vertical carbon flux (the marginal ice zone and open Barents Sea). J Mar Syst 38:147–164. doi:10.1016/s0924-7963(02)00174-4 CrossRefGoogle Scholar
  41. Pasternak A, Arashkevich E, Reigstad M, Wassmann P, Falk-Petersen S (2008) Dividing mesozooplankton into upper and lower size groups: applications to the grazing impact in the Marginal Ice Zone of the Barents Sea. Deep Sea Res Part II Top Stud Oceanogr 55:2245–2256. doi:10.1016/j.dsr2.2008.05.002 CrossRefGoogle Scholar
  42. Pasternak AF, Arashkevich EG, Grote U, Nikishina AB, Solovyev KA (2013) Different effects of increased water temperature on egg production of Calanus finmarchicus and C. glacialis. Oceanology 53:547–553. doi:10.1134/s0001437013040085 CrossRefGoogle Scholar
  43. Prosser CL (1961) Oxygen: respiration and metabolism. In: Prosser CL, Brown FA Jr (eds) Comparative animal physiology. Saunders WB, Philadelphia, pp 165–211Google Scholar
  44. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  45. Rall BC, Vucic-Pestic O, Ehnes RB, Emmerson M, Brose U (2010) Temperature, predator-prey interaction strength and population stability. Glob Change Biol 16:2145–2157. doi:10.1111/j.1365-2486.2009.02124.x CrossRefGoogle Scholar
  46. Reigstad M, Wassmann P (1996) Importance of advection for pelagic-benthic coupling in north Norwegian fjords. Sarsia 80:245–257Google Scholar
  47. Rey C, Carlotti F, Tande K, Hygum BH (1999) Egg and faecal pellet production of Calanus finmarchicus females from controlled mesocosms and in situ populations: influence of age and feeding history. Mar Ecol Prog Ser 188:133–148. doi:10.3354/meps188133 CrossRefGoogle Scholar
  48. Richardson AJ (2008) In hot water: zooplankton and climate change. ICES J Mar Sci 65:279–295. doi:10.1093/icesjms/fsn028 CrossRefGoogle Scholar
  49. Rohatgi A (2013) WebPlotDigitizer 2.6. http://arohatgi.info/WebPlotDigitizer
  50. Runge JA (1980) Effects of hunger and season on the feeding behavior of Calanus pacificus. Limnol Oceanogr 25:134–145CrossRefGoogle Scholar
  51. Saiz E, Calbet A (2007) Scaling of feeding in marine calanoid copepods. Limnol Oceanogr 52:668–675CrossRefGoogle Scholar
  52. Screen JA, Simmonds I (2010) The central role of diminishing sea ice in recent Arctic temperature amplification. Nature 464:1334–1337. doi:10.1038/nature09051 PubMedCrossRefGoogle Scholar
  53. Seuthe L, Darnis G, Riser CW, Wassmann P, Fortier L (2007) Winter-spring feeding and metabolism of Arctic copepods: insights from faecal pellet production and respiration measurements in the southeastern Beaufort Sea. Polar Biol 30:427–436. doi:10.1007/s00300-006-0199-1 CrossRefGoogle Scholar
  54. Tande KS (1988) The effects of temperature on metabolic rates of different life stages of Calanus glacialis in the Barents Sea. Polar Biol 8:457–461. doi:10.1007/bf00264722 CrossRefGoogle Scholar
  55. Tande KS, Båmstedt U (1985) Grazing rates of the copepods Calanus glacialis and Calanus finmarchicus in Arctic waters of the Barents Sea. Mar Biol 87:251–258. doi:10.1007/bf00397802 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Ulrike Grote
    • 1
  • Anna Pasternak
    • 2
  • Elena Arashkevich
    • 2
  • Elisabeth Halvorsen
    • 1
  • Anastasia Nikishina
    • 2
  1. 1.Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and EconomicsUiT The Arctic University of NorwayTromsøNorway
  2. 2.Shirshov Institute of OceanologyRASMoscowRussia

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