Skip to main content
Log in

Respiration and ammonia excretion by marine metazooplankton taxa: synthesis toward a global-bathymetric model

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

For thirteen representative taxa of metazooplankton from various depth horizons (<4,200 m) of the world’s oceans, respiration rate (681 datasets on 390 species) and ammonia excretion rate (266 datasets on 190 species) are compiled and analyzed as a function of body mass (dry mass, carbon or nitrogen), habitat temperature, habitat depth and taxon. Stepwise-regression analyses reveal that body mass is the most important parameter, followed by habitat temperature and habitat depth, whereas taxon is of lesser importance for both rates. The resultant multiple regression equations show that both respiration rate and ammonia excretion rate (per individual) increase with increase in body mass and habitat temperature, but decrease with habitat depth. Some taxa are characterized by significantly higher or lower rates of respiration or ammonia excretion than the others. Overall, the global-bathymetric models explain 93.4–94.2 % of the variance of respiration data and 80.8–89.7 % of the variance of ammonia excretion data. The atomic O:N ratios (respiration/ammonia excretion) are largely independent of body mass, habitat temperature, habitat depth and taxon, with a median of 17.8. The present results are discussed in light of the methodological constraints and the standing hypotheses for the relationship between metabolic rate and temperature. Perspectives for model improvement and possible application of it to plankton-imaging systems for rapid assessment of the role of metazooplankton in C or N cycles in the pelagic ecosystem are briefly discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agutter PS, Tuszynski JA (2011) Analytic theories of allometric scaling. J Exp Biol 214:1055–1062

    Article  Google Scholar 

  • Almeda R, Alcaraz M, Calbet A, Saiz E (2011) Metabolic rates and carbon budget of early developmental stages of the marine cyclopoi copepod Oithona davisae. Limnol Oceanogr 56:403–4146

    Article  CAS  Google Scholar 

  • Al-Mutairi H, Landry MR (2001) Active export of carbon and nitrogen at Station ALOHA by diel migrant zooplankton. Deep Sea Res II 48:2083–2103

    Article  CAS  Google Scholar 

  • Bailey TG, Torres JJ, Youngbluth MJ, Owen GP (1994) Effect of decompression on mesopelagic gelatinous zooplankton: a comparison of in situ and shipboard measurements of metabolism. Mar Ecol Prog Ser 113:13–27

    Article  Google Scholar 

  • Bailey TG, Youngbluth MJ, Owen GP (1995) Chemical composition and metabolic rates of gelatinous zooplankton from midwater and benthic boundary layer environments off Cape Hatteras, North Carolina, USA. Mar Ecol Prog Ser 122:121–134

    Article  CAS  Google Scholar 

  • Bailey DM, Bagley PM, Jamieson AJ, Cromarty A, Collins MA, Tselepidis A, Priede IG (2005) Life in a warm deep sea: routine activity and burst swimming performance of the shrimp Acanthephyra eximia in the abyssal Mediterranean. Mar Biol 146:1199–1206

    Article  Google Scholar 

  • Båmstedt U (1979) Seasonal variation in the respiratory rate and ETS activity of deep-water zooplankton from the Swedish west coast. In: Naylor E, Hartnoll RG (eds) Cyclic phenomena in marine plants and animals. Pergamon Press, Oxford, pp 267–274

    Chapter  Google Scholar 

  • Båmstedt U (1986) Chemical composition and energy content. In: Corner EDS, O’Hara SCM (eds) The biological chemistry of marine copepods. Clarendon Press, Oxford, pp 1–58

    Google Scholar 

  • Benfield MC, Grosjean P, Culverhouse PF, Irigoien X, Sieracki ME, Lopez-Urrutia A, Dam HG, Hu Q, Davies CS, Hansen A, Pilskaln CH, Riseman EM, Schlts H, Utgoff PE, Gorsky G (2007) RAPID, research on automated plankton identification. Oceanography 20:172–187

    Article  Google Scholar 

  • Biggs DC (1977) Respiration and ammonia excretion by open ocean gelatinous zooplankton. Limnol Oceanogr 22:108–117

    Article  CAS  Google Scholar 

  • Bokma (2004) Evidence against universal metabolic allometry. Funct Ecol 18:184–187

    Article  Google Scholar 

  • Brey T (2010) An empirical model for estimating aquatic invertebrate respiration. Method Ecol Evol 1:92–101

    Article  Google Scholar 

  • Buitenhuis E, Le Quere C, Aumont O, Beaugrand G, Bunker A, Hirst A, Ikeda T, O’Brien T, Pointkovski S, Straile D (2006) Biogeochemical fluxes through mesozooplankton. Global Biogeochem Cycles 20:1–18

    Article  Google Scholar 

  • Castellani C, Robinson C, Smith T, Lampitt RS (2005) Temperature affects respiration rate of Oithona similis. Mar Ecol Prog Ser 285:129–135

    Article  Google Scholar 

  • Census of Marine Zooplankton (CMarZ) (2004) Science plan ver 28 July 2004. Portsmouth, New Hampshire, pp 1–52

  • Cetta CM, Madin LP, Kremer P (1986) Respiration and excretion by oceanic salps. Mar Biol 91:529–537

    Article  Google Scholar 

  • Childress JJ (1975) The respiratory rates of midwater crustaceans as a function of depth occurrence and relation to the oxygen minimum layer off Southern California. Comp Biochem Physiol A 50:787–799

    Article  CAS  Google Scholar 

  • Childress JJ (1995) Are there physiological and biochemical adaptation of metabolism in deep-sea animals? Trends Ecol Evol 10:30–36

    Article  CAS  Google Scholar 

  • Clarke A (1987) The adaptation of aquatic animals to low temperatures. In: Grout BWW, Morris GJ (eds) The effects of low temperatures on biological systems. Edward Arnold, London, pp 315–348

    Google Scholar 

  • Clarke A (2006) Temperature and the metabolic theory of ecology. Funct Ecol 20:405–412

    Article  Google Scholar 

  • Clarke A, Fraser KPP (2004) Why does metabolism scale with temperature ? Funct Ecol 18:243–251

    Article  Google Scholar 

  • Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905

    Article  Google Scholar 

  • Culverhouse PF, Williams R, Benfield M, Flood PR, Sell AF, Mazzocchi MG, Buttino I, Sieracki M (2006) Automatic image analysis of plankton: future perspectives. Mar Ecol Prog Ser 312:287–309

    Article  Google Scholar 

  • Davis CS, Hu Q, Gallager SM, Tang X, Ashjian CJ (2004) Real-time observation of taxa-specific plankton distributions: an optical sampling method. Mar Ecol Prog Ser 284:77–96

    Article  Google Scholar 

  • Dodds PS, Rothman DH, Weitz JS (2001) Re-examination of the ‘3/4-law’ of metabolism. J Theor Biol 209:9–27

    Article  CAS  Google Scholar 

  • Donnelly J, Kawall H, Geiger SP, Torres JJ (2004) Metabolism of Antarctic micronektonic Crustacea across a summer ice-edge bloom: respiration, composition, and enzymatic activity. Deep-Sea Res II 51:2225–2245

    Article  CAS  Google Scholar 

  • Feigenbaum D (1991) Food and feeding. In: Bone Q, Kapp H, Pierrot-Bolts AC (eds) The biology of chaetognaths. Oxford University Press, Oxford, pp 45–54

    Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Gerber RP, Gerber MB (1979) Ingestion of natural particulate organic matter and subsequent assimilation, respiration and growth by tropical lagoon zooplankton. Mar Biol 52:33–44

    Article  Google Scholar 

  • Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251

    Article  CAS  Google Scholar 

  • Gillooly JF, Allen AP, Savage VM, Charnov EL, West GB, Brown JH (2006) Response to Clarke and Fraser: effects of temperature on metabolic rate. Funct Ecol 20:400–404

    Article  Google Scholar 

  • Gorsky G, Palazzoli I, Fenaux R (1987) Influence of temperature changes on oxygen uptake and ammonia and phosphate excretion, in relation to body size and weight, in Oikopleura dioica (Appendicularia). Mar Biol 94:191–201

    Article  Google Scholar 

  • Gorsky G, Ohman MD, Picheral M, Gasparini S, Stemmann L, Romagnan JB, Cawood A, Pesant S, Garcia-Comas C, Prejger F (2010) Digital zooplankton image analysis using the ZooScan integrated system. J Plankton Res 32:285–303

    Article  Google Scholar 

  • Grosjean P, Picheral M, Warembourg C, Gorsky (2004) Enumeration, measurement, and identification of net zooplankton samplings using the ZOOSCAN digital imaging system. ICES J Mar Sci 61:518–525

    Article  Google Scholar 

  • Hemmingsen AN (1960) Energy metabolism as related to body size and respiratory surfaces, and its evolution. Rep Steno meml Hosp 9:1–110

    Google Scholar 

  • Hernández-León S, Ikeda T (2005) A global assessment of mesozooplankton respiration in the ocean. J Plankton Res 27:153–158

    Article  Google Scholar 

  • Hidaka K, Kawaguchi K, Murakami M, Takahashi M (2001) Downward transport of organic carbon by diel migratory micronekton in the western equatorial Pacific: its quantitative and qualitative importance. Deep Sea Res I 48:1923–1939

    Article  CAS  Google Scholar 

  • Hirche H-J (1984) Temperature and metabolism of plankton-I. Respiration of Antarctic zooplankton at different temperatures with a comparison of Antarctic and Nordic krill. Comp Biochem Physiol 77A:361–368

    Article  Google Scholar 

  • Hirche H-J (1987) Temperature and plankton-II. Effect on respiration and swimming in copepods from the Greenland Sea. Mar Biol 94:347–356

    Article  Google Scholar 

  • Iguchi N, Ikeda T (2004) Metabolism and elemental composition of aggregate and solitary forms of Salpa thompsoni (Tunicate: Thaliacea) in waters off the Antarctic Peninsula during austral summer 1999. J Plankton Res 26:1025–1037

    Article  CAS  Google Scholar 

  • Ikeda T (1974) Nutritional ecology of marine zooplankton. Mem Fac Fish Hokkaido Univ 22:1–97

    Google Scholar 

  • Ikeda T (1985) Metabolic rates of epipelagic marine zooplankton as a function of body mass and temperature. Mar Biol 85:1–11

    Article  Google Scholar 

  • Ikeda T (1988) Metabolism and chemical composition of crustaceans from the Antarctic mesopelagic zone. Deep Sea Res 35:1991–2002

    Article  CAS  Google Scholar 

  • Ikeda T (1989) Are antarctic zooplankton metabolically more cold-adapted than arctic zooplankton? An intra-generic comparison of oxygen consumption rates. J Plankton Res 11:619–624

    Article  Google Scholar 

  • Ikeda T (1990) Ecological and biological features of a mesopelagic ostracod, Conchoecia pseudodiscophora, in the Japan Sea. Mar Biol 107:453–461

    Article  Google Scholar 

  • Ikeda T (2008) Metabolism in mesopelagic and bathypelagic copepods: Reply to Childress et al. (2008). Mar Ecol Prog Ser 373:193–196

    Article  Google Scholar 

  • Ikeda T (2012) Metabolism and chemical composition of zooplankton from 500 to 5,000 m depth of the western subarctic Pacific Ocean. J Oceanogr 68:641–649

    Article  CAS  Google Scholar 

  • Ikeda T (2013a) Respiration and ammonia excretion of euphausiid crustaceans: synthesis towards a global-bathymetric model. Mar Biol 160:251–262

    Article  CAS  Google Scholar 

  • Ikeda T (2013b) Metabolism and chemical composition of marine pelagic amphipods: synthesis towards a global-bathymetric model. J Oceanogr 69:339–355

    Article  CAS  Google Scholar 

  • Ikeda T (2013c) Synthesis toward a global-bathymetric model of metabolism and chemical composition of mysid crustaceans. J Exp Mar Biol Ecol 445:79–87

    Article  CAS  Google Scholar 

  • Ikeda T (2013d) Metabolism and chemical composition of pelagic decapods shrimps: synthesis toward a global-bathymetric model. J Oceanogr 69:671–686

    Article  Google Scholar 

  • Ikeda T (2014a) Synthesis toward a global model of metabolism and chemical composition of medusae and ctenophores. J Exp Mar Biol Ecol 456:50–64

    Article  CAS  Google Scholar 

  • Ikeda T (2014b) Metabolism and chemical composition of marine pelagic gastropod mullucs: a synthesis. J Oceanogr 70:289–305

    Article  CAS  Google Scholar 

  • Ikeda T, Bruce B (1986) Metabolic activity and elemental composition of krill and other zooplankton from Prydz Bay, Antarctica, during early summer (November–December). Mar Biol 92:545–555

    Article  CAS  Google Scholar 

  • Ikeda T, Kirkwood R (1989) Metabolism and elemental composition of a giant chaetognath Sagitta gazellae from the Southern Ocean. Mar Biol 100:261–267

    Article  CAS  Google Scholar 

  • Ikeda T, McKinnon AD (2012) Metabolism and chemical composition of zooplankton and hyperbenthos from the Great Barrier Reef waters, North Queensland, Australia. Plankton Benthos Res 7:8–19

    Article  Google Scholar 

  • Ikeda T, Mitchell AW (1982) Oxygen uptake, ammonia excretion, and phosphate excretion of krill and other Antarctic zooplankton, in relation to their body size and chemical composition. Mar Biol 71:283–298

    Article  Google Scholar 

  • Ikeda T, Motoda S (1978) Estimated zooplankton production and their ammonia excretion in Kuroshio and adjacent seas. Fish Bull US 76:357–367

    CAS  Google Scholar 

  • Ikeda T, Skjoldal HR (1989) Metabolism and elemental composition of zooplankton from the Barents Sea during early arctic summer. Mar Biol 100:173–183

    Article  CAS  Google Scholar 

  • Ikeda T, Takahashi T (2012) Synthesis towards a global-bathymetric model of metabolism and chemical composition of marine pelagic chaetognaths. J Exp Mar Biol Ecol 424–425:78–88

    Article  Google Scholar 

  • Ikeda T, Torres JJ, Hernández-León S, Geiger SP (2000) Metabolism. In: Harris RP, Wiebe PH, Lenz J, Skjoldal HR, Huntley M (eds) ICES zooplankton methodology manual. Academic Press, San Diego, pp 455–532

    Chapter  Google Scholar 

  • Ikeda T, Kanno 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

    Google Scholar 

  • Ikeda T, Sano F, Yamaguchi A, Matsuishi T (2006a) Metabolism of mesopelagic and bathypelagic copepods in the western North Pacific Ocean. Mar Ecol Prog Ser 322:199–211

    Article  CAS  Google Scholar 

  • Ikeda T, Yamaguchi A, Matsuishi T (2006b) Chemical composition and energy content of deep-sea calanoid copepods in the western North Pacific Ocean. Deep Sea Res I 53:1791–1809

    Article  Google Scholar 

  • Ikeda T, Sano F, Yamaguchi A (2007) Respiration in marine pelagic copepods: a global-bathymetric model. Mar Ecol Prog Ser 339:215–219

    Article  Google Scholar 

  • Ivleva IV (1980) The dependence of crustacean respiration rate on body mass and habitat temperature. Int Revue Ges Hydrobiol 65:1–47

    Article  Google Scholar 

  • Kaeriyama H, Ikeda T (2004) Metabolism and chemical composition of mesopelagic ostracods in the western North Pacific Ocean. ICES J Mar Sci 61:535–541

    Article  CAS  Google Scholar 

  • Köster M, Paffenhöfer G-A, Baker CV, Williams JE (2010) Oxygen consumption of doliolids (Tunicata, Thaliacea). J Plankton Res 32:171–180

    Article  Google Scholar 

  • Kozłowski J, Konarzewski M (2004) Is West, Brown and Enquist’s model of allometric scaling mathematically correct and biologically relevant? Functional Ecol 18:283–289

    Article  Google Scholar 

  • Kozłowski J, Konarzewski M (2005) West, Brown and Enquist’s model of allometric scaling again: the same questions remain. Funct Ecol 19:739–743

    Article  Google Scholar 

  • Kruse S, Brey T, Bathmann U (2010) Role of midwater chaetognaths in Southern Ocean pelagic energy flow. Mar Ecol Prog Ser 416:105–113

    Article  Google Scholar 

  • Kutner MH, Nachtsheim C, Neter C (2004) Applied linear regression models, Forth edn. McGraw-Hill, Irwin

    Google Scholar 

  • Lee RF, Hagen W, Kattner G (2006) Lipid storage in marine zooplankton. Mar Ecol Prog Ser 307:273–306

    Article  CAS  Google Scholar 

  • Lehette P, Hernández-León S (2009) Zooplankton biomass estimation from digitized image: a comparison between subtropical and Antarctic organisms. Limnol Oceanogr Methods 7:304–308

    Article  Google Scholar 

  • Lombard F, Sciandra A, Gorsky G (2005) Influence of body mass, food concentraton, temperature and filtering activity on the oxygen uptake of the appendicularian Oikopleura dioica. Mar Ecol Prog Ser 301:149–158

    Article  Google Scholar 

  • López-Urrutia Á, Martin ES, Harris RP, Irigoien X (2006) Scaling the metabolic balance of the oceans. Proc Natl Acad Sci 103:8739–8744

    Article  Google Scholar 

  • Madin LP, Purcell JE (1992) Feeding, metabolism, and growth of Cyclosalpa bakeri in the subarctic Pacific. Limnol Oceanogr 37:1236–1251

    Article  Google Scholar 

  • Mauchline J, Fisher LR (1967) The biology of euphausiids. Adv Mar Biol 7:1–454

    Google Scholar 

  • Mayzaud P, Dallot S (1973) Respiration et excrétion azotée du zooplankton. I. Evaluation des niveaux métaboliques de quelques espèces de Méditerranee occidentale. Mar Biol 19:307–314

    Article  CAS  Google Scholar 

  • Mukai H, Koike I, Nishihira M, Nojima S (1989) Oxygen consumption and ammonia excretion of mega-sized benthic invertebrates in a tropical seagrass bed. J Exp Mar Biol Ecol 134:101–115

    Article  Google Scholar 

  • Musayeva EI, Shushkina EA (1978) Metabolic rates of planktonic animals living at different temperature. Oceanology 18:343–346

    Google Scholar 

  • Nival P, Nival S, Palazzoli I (1972) Données sur la respiration de différents organismes communs dans le plancton de Villefranche-sur-Mer. Mar Biol 17:63–76

    Google Scholar 

  • Omori M, Ikeda T (1984) Methods in marine zooplankton ecology. Wiley, New York

    Google Scholar 

  • Postel L, Fock H, Hagen W (2000) Biomass and abundance. In: Harris RP, Wiebe PH, Lenz J, Skjoldal HR, Huntley M (eds) ICES zooplankton methodology manual. Academic Press, San Diego, pp 83–192

    Chapter  Google Scholar 

  • Purcell JE (1991) A review of cnidarians and ctenophores feeding on competitors in the plankton. Hydrobiologia 216:335–342

    Article  Google Scholar 

  • Quetin LB, Ross RM, Uchio K (1980) Metabolic characteristics of midwater zooplankton: ammonia excretion, O:N ratios, and the effect of starvation. Mar Biol 59:201–209

    Article  CAS  Google Scholar 

  • Reeve MR, Raymont JEG, Raymont JKB (1970) Seasonal biochemical composition and energy sources of Sagitta hispida. Mar Biol 6:357–364

    Article  CAS  Google Scholar 

  • Roger C (1988) Recyclage des sels nutritifs par le macroplancton-micronecton dans le Pacifique tropical Sud-Ouest. Oceanol Acta 11:107–116

    CAS  Google Scholar 

  • Schneider G (1990) A comparison of carbon based ammonia excretion rates between gelatinous and non-gelatinous zooplankton: implications and consequences. Mar Biol 106:219–225

    Article  CAS  Google Scholar 

  • Secor SM (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179:1–56

    Article  Google Scholar 

  • Seibel BA, Drazen JC (2007) The rate of metabolism in marine animals: environmental constraints, ecological demands and energetic opportunities. Phil Trans R Soc B 362:2061–2078

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. The principles and practice of statistics in biological research, Freeman, New York

    Google Scholar 

  • Svetlichny LS, Hubareva ES, Erkan F, Gucu AC (2000) Physiological and behavioral aspects of Calanus euxinus femals (Copepoda: Calanoida) during vertical migration across temperature and oxygen gradients. Mar Biol 137:963–971

    Article  Google Scholar 

  • Szyper JP (1981) Short-term starvation effects on nitrogen and phosphorus excretion by the chaetognath Sagitta enflata. Estuar cstl Shelf Sci 13:691–700

    Article  CAS  Google Scholar 

  • Thor P (2002) Specific dynamic action and carbon incorporation in Calanus finmarchcus copepodites and females. J Exp Mar Biol Ecol 272:159–169

    Article  CAS  Google Scholar 

  • Thuesen EV, Childress JJ (1993) Metabolic rates, enzyme activities and chemical composition of some deep-sea pelagic worms, particularly Nectonemertes mirabilis (Nemertea; Hoplonemertinea) and Poeobius meseres (Annelida; Polychaeta). Deep-Sea Res 1(40):937–951

    Article  Google Scholar 

  • Torres JJ, Aarset AV, Donnelly J, Hopkins TL, Lancraft TM, Ainley DJ (1994) Metabolism of Antarctic micronektonic Crustacea as a function of depth of occurrence and season. Mar Ecol Prog Ser 113:207–219

    Article  Google Scholar 

  • Vernon HM (1896) The respiratory exchange of the lower marine invertebrates. J Physiol 19:18–70

    Google Scholar 

  • Vidal J, Whitledge TE (1982) Rates of metabolism of planktonic crustaceans as related to body weight and temperature of habitat. J Plankton Res 4:77–84

    Article  Google Scholar 

  • West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276:122–126

    Article  CAS  Google Scholar 

  • Yamaguchi A, Watanabe Y, Ishida H, Harimoto T, Furusawa K, Suzuki S, Ishizaka J, Ikeda T, Takahashi MM (2002) Community and trophic structures of pelagic copepods down to greater depths in the western subarctic Pacific (WEST-COSMIC). Deep-Sea Res I 49:1007–1025

    Article  Google Scholar 

Download references

Acknowledgments

I am grateful to Charlie Miller for editing and constructive comments on early drafts of this paper. Thanks are due to three anonymous referees for their comments which improved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tsutomu Ikeda.

Additional information

Communicated by X. Irigoyen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 183 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ikeda, T. Respiration and ammonia excretion by marine metazooplankton taxa: synthesis toward a global-bathymetric model. Mar Biol 161, 2753–2766 (2014). https://doi.org/10.1007/s00227-014-2540-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-014-2540-5

Keywords

Navigation