Abstract
The study of the structural and functional properties of key components of polar marine ecosystems has received increased attention in order to better understand the ecological consequences of future sea temperature rise and seasonal ice retraction. Owing to this purpose, during the ATOS-Arctic cruise, held in July 2007 in the framework of the 2007–2008 International Polar Year, we studied the respiratory carbon demand of mesozooplankton as well as their contribution to the regeneration of inorganic nitrogen and phosphorus (NH4-N and PO4-P) via excretion. The studied area comprised several stations along a latitudinal gradient in the East Greenland current, plus a network of stations NW of the Svalbard islands. The specific respiratory carbon losses and phosphorus (PO4-P) excretion rates were similar or slightly higher than some reports for Arctic mesozooplankton, but the nitrogen (NH4-N) excretion rates were higher by a factor of 3 when compared with previous data sets. The mesozooplankton respiratory losses were equivalent to 23% of primary production, and at turn zooplankton contributed by excretion to more than 50% of the N and P required by phytoplankton. Although C:N, C:P and N:P metabolic atomic quotients almost coincided with the average Redfield’s stoichiometric ratios, the low C:N values when compared to previous reports suggested a predominance of protein-related metabolic substrates. The potential consequences of changes observed in the C:N, N:P and C:P metabolic ratios of mesozooplankton for Arctic marine ecosystems are discussed.
Similar content being viewed by others
References
Alcaraz M (1974) Respiración en crustáceos: influencia de la concentración de oxígeno en el medio. Inv Pesq 38:397–411
Alcaraz M (1988) Summer zooplankton metabolism and its relation to primary production in the western Mediterranean. Oceanol Acta 9:185–191
Alcaraz M (1997) Copepods under turbulence: grazing, behavior and metabolic rates. In: Marrasé C and Saiz E (eds) Lectures on plankton and turbulence. Sci Mar 61:177–195
Alcaraz M, Saiz E, Fernandez JA, Trepat I, Figueiras F, Calbet A, Bautista B (1998) Antarctic zooplankton metabolism: carbon requirements and ammonium excretion of salps and crustacean zooplankton in the vicinity of the Bransfield strait during January 1994. J Mar Syst 17:347–359
Alcaraz M, Saiz E, Calbet A, Fernandez JA, Trepat I, Broglio E (2003) Estimating zooplankton biomass through image analysis. Mar Biol 143:307–315
Auel H, Hagen W (2002) Mesozooplankton community structure abundance and biomass in the central Arctic Ocean. Mar Biol 140:1013–1021
Bamstedt U, Tande KS (1985) Respiration and excretion rates of Calanus glacialis in Arctic waters of the Barents Sea. Mar Biol 87:295–296
Böttger R, Schnack D (1986) On the effect of formaldehyde fixation on the dry weight of copepods. Meeresforschung 31:141–152
Carmack E, Barber D, Christensen J, Macdonald R, Rudels B, Sakshaug E (2006) Climate variability and physical forcing on the food webs and the carbon budget on panarctic shelves. Prog Oceanogr 71:145–182
Comiso JC, Parkinson CL, Gersten R, Stock R (2008) Accelerated decline in the Arctic sea ice cover. Geophys Res Lett 35:L01703
Conover RJ (1960) The feeding behavior and respiration of some marine planktonic crustacea. Biol Bull 119:399–415
Conover RJ, Corner EDS (1968) Respiration and nitrogen excretion by some marine zooplankton in relation to their life cycles. J Mar Biol Ass UK 48:49–75
Conover RJ, Gustavson KR (1999) Source of urea in arctic seas: zooplankton metabolism. Mar Ecol Prog Ser 179:41–54
Conover RJ, Huntley M (1991) Copepod in ice-covered seas- Distribution adaptations to seasonally limited food metabolism growth patterns and life cycle strategies in polar seas. J Mar Systems 2:1–41
Corner EDS, Davies AG (1971) Plankton as factor in the nitrogen and phosphorus cycles in the sea. Adv Mar Biol 9:101–204
Duarte CM (ed) (2008) Impacts of global warming on polar ecosystems. Fundación BBVA Bilbao
Duarte CM, Lasternas S, Agustí S, Regaudie-de-Gioux A, Echeveste P, Tovar-Sánchez A, Arrieta JM, Álvarez M, Dachs J, Lacorte S, Tauler R, Galbán C, Berrojariz N (in revision) Ice Melting Suppresses Primary Production in the Arctic Ocean. Science
Fernandes JA, Irigoien X, Boyra G, Lozano JA, Albaina A (2009) Optimizing the number of classes in automated zooplankton classification. J Plankton Res 31:19–29
Gislason A, Astthorsson OS (1998) Seasonal variations in biomass abundance and composition of zooplankton in the subarctic waters north of Iceland. Polar Biol 20:85–94
Grasshoff K, Kremling K, Ehrhardt M (1999) Methods of seawater analysis. Wiley, VCH
Grosjean P, Picheral M, Warembourg C (2004) Enumeration measurement and identification of net zooplankton samples using the ZOOSCAN digital imaging system. ICES J Mar Sci 61:518–525
Hansen B, Verity P, Falkenhaug T, Tande KS, Norrbin F (1994) On the trophic fate of Phaeocystis pouchetti (Harriot). V. Trophic relationships between Phaeocystis and zooplankton: an assessment of methods and size dependence. J Plankton Res 16:487–511
Harris E (1959) The nitrogen cycle in Long Island Sound. Bull Bingham Oceanogr Coll 17:31–65
Harris E, Riley GA (1956) Oceanography of Long Island Sound 1952–1954. VIII. Chemical composition of the plankton. Bull Bingham Oceanogr Coll 15:315–323
Hirche HJ (1987) Temperature and plankton. II. Respiration and swimming activity of copepods from the Greenland Sea at different temperatures. Mar Biol 94:347–356
Hirche HJ, Baumann MEM, Kattner G, Gradinger R (1991) Plankton distribution and the impact of copepod grazing on primary production in Fram Strait, Greenland Sea. J Mar Systems 2:477–494
Hjort J (1914) Fluctuations in the great fisheries viewed in the light of biological research. Rapp P Verb Réun Cons Int Explor Mer 20:1–13
Hobson KA, Fisk A, Karnovsky N, Holst M, Gagnon JM, Fortier M (2002) A stable isotope (∂13C, ∂15N) model for the North Water food web: implications for evaluating trophodynamics and the flow of energy and contaminants. Deep Sea Res II 49:5131–5150
Hopkins TL (1969) Zooplankton standing crop in the Arctic basin. Limnol Oceanogr 14:80–85
Huntley M, Tande K, Eilestsen HC (1987) On the trophic fate of Phaeocystis pouchetti (Hariot) II. Grazing rates of Calanus hyperboreus (Kroyer) on diatoms and different size categories of Phaeocystis pouchetti. J Exp Mar Biol Ecol 110:197–212
Ikeda T (1977) The effect of laboratory conditions on extrapolations of experimental measurements to the ecology of marine zooplankton. IV: Changes in respiration and excretion rates of boreal zooplankton species maintained under fed and starved conditions. Mar Biol 41:241–252
Ikeda T, Skjoldal HR (1989) Metabolism and elemental composition of zooplankton from the Barents Sea during early Arctic summer. Mar Biol 100:173–183
Ikeda T, Fay H, Hutchinson SA, Boto GM (1982) Ammonia and inorganic phosphate excretion by zooplankton from inshore waters of the Great Barrier Reef, Queensland. I. Relationships between excretion and body size. Austr J Mar Freshw Res 33:55–70
Ikeda T, Kano Y, Ozaki K, Shinada A (2001) Metabolic rates of epipelagic marine copepods as a function of body mass and temperature. Mar Biol 139:587–596
Kéruel R, Aminot A (1997) Fluorometric determination of ammonia in sea and estuarine waters by direct segmented flow analysis. Mar Chem 57:265–275
Lasternas S and Agusti S. Phytoplankton production and community structure during the arctic ice-melting record in summer 2007. (this volume)
Le Borgne R (1977) Étude de la production pélagique de la zone équatoriale de l’Atlantique à 4º WW. III. Respiration et excretion d’azote et de phosphore du zooplankton. Cah ORSTOM Ser Océanogr 15:349–362
Levinsen H, Tuenr JT, Nielsen TG, Hansen BW (2000) On the trophic coupling between protists and copepods in arctic marine ecosystems. Mar Ecol Prog Ser 204:65–77
Loeng H, Drinkwater K (2007) An overview of the ecosystems of the Barents and Norwegian Seas and their response to climate variability. Deep-Sea Res II 54:2478–2500
Mayzaud P (1973) Respiration and nitrogen excretion of zooplankton. II. Studies of the metabolic characteristics of starved animals. Mar Biol 21:19–28
Mayzaud P (1976) Respiration and nitrogen excretion of zooplankton. IV. The influence of starvation on the metabolism and the biochemical composition of some species. Mar Biol 37:47–58
Mayzaud P, Conover RA (1988) O:N atomic ratio as a tool to describe zooplankton metabolism. Mar Ecol Prog Ser 45:289–302
Møller EF, Nielsen GT and Richardson K (2006) The zooplankton community in the Greenland Sea: composition and role in carbon turnover. Deep-Sea Res I:76–93
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
Noji TT, Rey F, Miller LA, Borsheim KI, Urban-Rich J (1999) Fate of biogenic carbon in the upper 200 m of the central Greenland Sea. Deep Sea Res II 46:1497–1509
Olli K, Wassmann P, Reigstad M, Ratkova T, Arashkevich E, Pasternak A, Matrai PA, Knulst J, Tranvik L, Klais R, Jacobsen A (2007) The fate of production in the central Arctic Ocean–top-down regulation by zooplankton expatriates? Prog Oceanogr 72:84–113
Omori M (1978) Some factors affecting on dry weight, organic weight and concentration of carbon and nitrogen in freshly prepared and in preserved zooplankton. Int Rev Ges Hydrobiol 63:261–269
Omori M, Ikeda T (1984) Methods in zooplankton ecology. John Wiley and son
Redfield AC, Ketchum BH, Richards FA (1963) The influence of organisms on the composition of seawater. In: the Sea. Ideas and Observations on Progress in the Study of the Seas, MN Hill, NY, pp 26–77
Richardson K, Markager S, Buch E, Lassen MF, Kristensen AJ (2005) Seasonal distribution of primary production, phytoplankton biomass and size distribution in the Greenland Sea. Deep Sea Res I 52:979–999
Ricker WE (1973) Linear regression in fishery research. J Fish Res Bd Can 30:409–434
Rudels B, Björk G, Nilsson J, Winsor P, Lake I, Nohr C (2005) The interaction between waters from the Arctic Ocean and the Nordic Seas of Fram Strait and along the East Greenland Current: results from the Arctic Ocean-02 Oden expedition. J Mar Systems 55:1–30
Saba GK, Steinberg DK, Bronk DA (2009) Effects of diet on release of dissolved organic and inorganic nutrients by the copepod Acartia tonsa. Mar Ecol Prog Ser 386:147–161
Skjoldal HR, Bamsted U, Klinken J, Laing A (1984) Changes with time after capture in the metabolic activity of the carnivorous copepod Euchaeta norvegica Boeck. J Exp Mar Biol Ecol 83:195–210
Smetacek V, Nicol S (2005) Polar ocean ecosystems in a changing world. Nature 437:362–368
Steemann-Nielsen EJ (1952) The use of radio-active carbon (Cl4) for measuring organic production in the sea. Cons Perm Int Explor Mer 18:117–140
Sterner RW (1986) Herbivores’ direct and indirect effect on algal populations. Science 231:605–607
Sterner RW (1990) The ratio of nitrogen to phosphorus ressuplied by herbivores: Zooplankton and the algal arena. Am Nat 136:209–229
Stevens CJ, Deibel D, Parrish C (2004) Copepod omnivory in the North Water Polynya (Baffin Bay) during autumn: spatial pattern in lipid composition. Deep Sea Res I 51:1637–1639
Tamelander T, Reigstad M, Hop H, Carroll ML, Wasmann P (2008) Pelagic and sympagic contribution of organic matter to zooplankton and vertical export in the Barents Sea marginal ice zone. Deep Sea II 55:2330–2339
Thibault D, Head E, Wheeler A (1999) Mesozooplankton in the Arctic Ocean in summer. Deep Sea Res I 46:1391–1415
Wassmann P, Carroll J, Bellerby RGJ (2008) Carbon flux and ecosystem feedback in the northern Barents Sea in an era of climate change. Deep Sea Res II 55
Yentsch CS, Menzel DW (1963) A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. Deep Sea Res 10:221–231
Acknowledgments
The authors are indebted to all the participants to the ATOS-Arctic cruise and particularly to the crew of the BIO “Hespérides” and the technical staff of the UTM (CSIC). P. Jimenez and E. Velasco contributed to the analysis of zooplankton biomass, and X. Irigoien and J.A. Fernandes gave valuable suggestions for the use of ZooImage® software. This research was supported by the Spanish grants POL2006-0550/CTM to C. D, CTM2006-12344-C02-01 to M. A., 2005SGR-00219 from the Generalitat de Catalunya to M. A, A. C. and E. S., and a PhD fellowship, BES-2005-7491 to RA.
Author information
Authors and Affiliations
Corresponding author
Additional information
This article belongs to the special issue: Impacts of climate warming on marine and freshwater Polar ecosystems, coordinated by S. Agustí, M. Sejr, and C. M. Duarte.
Rights and permissions
About this article
Cite this article
Alcaraz, M., Almeda, R., Calbet, A. et al. The role of arctic zooplankton in biogeochemical cycles: respiration and excretion of ammonia and phosphate during summer. Polar Biol 33, 1719–1731 (2010). https://doi.org/10.1007/s00300-010-0789-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-010-0789-9