Skip to main content

Advertisement

Log in

Gelatinous and soft-bodied zooplankton in the Northeast Pacific Ocean: Phosphorus content and potential resilience to phosphorus limitation

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Marine ecosystems on continental shelves face multiple challenges due to anthropogenic disturbances, many of which can change the seawater stoichiometry (C:N:P) and consequently elemental ratios of phytoplankton. This change in food quality may not be tolerated by all grazers and predators. Gelatinous and soft-bodied zooplankton (GZ) might be more resilient to such changes. We sampled GZ species in neritic and oceanic waters of the Northeast Pacific off British Columbia, Canada, determined their phosphorus (P) content and elemental ratios (C/P, N/P), and analysed intraspecific variability associated with size and ontogeny. P content was measured for twelve GZ taxa. P % DW (dry weight) decreased with size for the hydrozoan Aequorea sp., scyphozoans Aurelia labiata, Cyanea capillata, and the thaliacean Salpa aspera, and differed significantly for two development stages of the salp S. aspera. While C/P and N/P were mostly size and stage independent, they were highly variable. C/P values of GZ were generally higher than values of crustacean zooplankton, indicating that GZ represent poor-quality prey for non-GZ predators, and that GZ may have a higher resilience towards P-limited (low quality) prey. Changing ocean conditions and nutrient stoichiometry of prey may favour GZ, although large variability in P dynamics among GZ taxa and uncertainty about future ocean stoichiometry changes make generalisations difficult.

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
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

Raw data have been deposited in PANGAEA (https://doi.org/10.1594/PANGAEA.933356).

References

  • Arai, M. N. & J. R. Jacobs, 1980. Interspecific predation of common Strait of Georgia planktonic Coelenterates: laboratory evidence. Canadian Journal of Fisheries and Aquatic Sciences 37: 120–123.

    Article  Google Scholar 

  • Bates, D. M., M. Maechler, B. Bolker & S. Walker, 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67(1): 1–48.

    Article  Google Scholar 

  • Beers, J. R., 1966. Studies on the chemical composition of the major zooplankton groups in the Sargasso Sea off Bermuda. Limnology and Oceanography 11(4): 520–528.

    Article  CAS  Google Scholar 

  • Blanchet, M., O. Pringault, M. Bouvy, P. Catala, L. Oriol, J. Caparros, E. Ortega-Retuerta, L. Intertaglia, N. West, M. Agis, P. Got & F. Joux, 2015. Changes in bacterial community metabolism and composition during the degradation of dissolved organic matter from the jellyfish Aurelia aurita in a Mediterranean coastal lagoon. Environmental Science and Pollution Research 22: 13638–13653.

    Article  CAS  PubMed  Google Scholar 

  • Boero, F., J. Bouillon, C. Gravili, M. P. Miglietta, T. Parsons & S. Piraino, 2008. Gelatinous plankton: irregularities rule the world (sometimes). Marine Ecology Progress Series 356: 299–310.

    Article  Google Scholar 

  • Boersma, M., N. Aberle, F. M. Hantzsche, K. Schoo, K. H. Wiltshire & A. M. Malzahn, 2008. Nutritional limitation travels up the food chain. International Review of Hydrobiology 93: 479–488.

    Article  Google Scholar 

  • Borodkin, S. O. & L. I. Korzhikova, 1991. The chemical composition of the ctenophore Mnemiopsis leidyi and its role in the nutrient transformation in the Black Sea. Okeanologiya 31(5): 754–758.

    CAS  Google Scholar 

  • Brotz, L., W. W. L. Cheung, K. Kleisner, E. A. Pakhomov & D. Pauly, 2012. Increasing jellyfish populations: trends in Large Marine Ecosystems. Hydrobiologia 690: 3–20.

    Article  Google Scholar 

  • Chen, L. & C. Li, 2017. Different tolerances of jellyfish ephyrae (Aurelia sp.1) and fish larvae (Paralichthys olivaceus) to nutrient limitations. Marine Ecology Progress Series 569: 1–13.

    Article  CAS  Google Scholar 

  • Chi, X., J. Dierking, H.-J.T. Hoving, F. Lüskow, A. Denda, B. Christiansen, U. Sommer, T. Hansen & J. Javidpour, 2021. Tackling the jelly web: trophic ecology of gelatinous zooplankton in oceanic food webs of the eastern tropical Atlantic assessed by stable isotope analysis. Limnology and Oceanography 66(2): 289–305.

    Article  CAS  Google Scholar 

  • Choy, C. A., S. H. D. Haddock & B. H. Robison, 2017. Deep pelagic food web structure as revealed by in situ feeding observations. Proceedings of the Royal Society B 284: 20172116.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chuard, P. J. C., M. D. Johnson & F. Guichard, 2019. Ocean acidification causes mortality in the medusa stage of the cubozoan Carybdea xaymacana. Scientific Reports 9: 5622.

    Article  PubMed  PubMed Central  Google Scholar 

  • Condon, R. H., M. W. Graham, C. M. Duarte, K. A. Pitt, C. H. Lucas, S. H. D. Haddock, K. R. Sutherland, K. L. Robinson, M. N. Dawson, M. B. Decker, C. E. Mills, J. E. Purcell, A. Malej, H. W. Mianzan, S.-I. Uye, S. Gelcich & L. P. Madin, 2012. Questioning the rise of gelatinous zooplankton in the world’s oceans. BioScience 62(2): 160–167.

    Article  Google Scholar 

  • Condon, R. H., C. M. Duarte, K. A. Pitt, K. L. Robinson, C. H. Lucas, K. R. Sutherland, H. W. Mianzan, M. Bogeberg, J. E. Purcell, M. B. Decker, S.-I. Uye, L. P. Madin, R. D. Brodeur, S. H. D. Haddock, A. Malej, G. D. Parry, E. Eriksen, J. Quinones, M. Acha, M. Harvey, J. M. Arthur & W. M. Graham, 2013. Recurrent jellyfish blooms are a consequence of global oscillations. PNAS 110(3): 1000–1005.

    Article  CAS  PubMed  Google Scholar 

  • Conley, K. R., F. Lombard & K. R. Sutherland, 2018. Mammoth grazers on the ocean’s minuteness: a review of selective feeding using mucous meshes. Proceedings of the Royal Society B 285: 20180056.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cripps, G., K. J. Flynn & P. L. Lindeque, 2016. Ocean acidification affects the phyto-zooplankton trophic transfer efficiency. PLoS ONE 11(4): e0151739.

    Article  PubMed  PubMed Central  Google Scholar 

  • Curl, H., Jr., 1962. Standing crops of carbon, nitrogen, and phosphorus and transfer between trophic levels, in continental shelf waters of New York. Rappt. Proces-Verbaux Reunions, Conseil Perm. Intern. Exploration Mer 153: 183–189.

    CAS  Google Scholar 

  • Dadon-Pilosof, A., F. Lombard, A. Genin, K. R. Sutherland & G. Yahel, 2019. Prey taxonomy rather than size determines salp diets. Limnology and Oceanography 64(5): 1996–2010.

    Article  Google Scholar 

  • Diaz, R. J. & R. Rosenberg, 2008. Spreading dead zones and consequences for marine ecosystems. Science 321(5891): 926–929.

    Article  CAS  Google Scholar 

  • Dubischar, C. D., E. A. Pakhomov, L. von Harbou, B. P. V. Hunt & U. V. Bathmann, 2012. Salps in the Lazarev Sea, Southern Ocean: II. Biochemical composition and potential prey value. Marine Biology 159(1): 15–24.

    Article  CAS  Google Scholar 

  • Elser, J. J., D. R. Dobberfuhl, N. A. Mackay & J. H. Schampel, 1996. Organism size, life history, and N: P stoichiometry. BioScience 46(9): 674–684.

    Article  Google Scholar 

  • Emadodin, I., T. Reinsch, A. Rotter, M. Orlando-Bonaca, F. Taube & J. Javidpour, 2020. A perspective on the potential of using marine organic fertilizers for the sustainable management of coastal ecosystem services. Environmental Sustainability 3: 105–115.

    Article  Google Scholar 

  • Finkel, Z. V., J. Beardall, K. J. Flynn, A. Quigg, T. A. V. Rees & J. A. Raven, 2010. Phytoplankton in a changing world: cell size and elemental stoichiometry. Journal of Plankton Research 32(1): 119–137.

    Article  CAS  Google Scholar 

  • Grasshoff, K., K. Kremling & M. Ehrhardt, 1999. Methods of Seawater Analysis, Wiley, New York:

    Book  Google Scholar 

  • Guy-Haim, T., M. Rubin-Blum, E. Rahav, N. Belkin, J. Silverman & G. Sisma-Ventura, 2020. The effects of decomposing invasive jellyfish on biogeochemical fluxes and microbial dynamics in an ultra-oligotrophic sea. Biogeosciences 17: 5489–5511.

    Article  CAS  Google Scholar 

  • Haigh, R., D. Ianson, C. A. Holt, H. E. Neate & A. M. Edwards, 2015. Effects of ocean acidification on temperate coastal marine ecosystems and fisheries in the Northeast Pacific. PLoS ONE 10(2): e0117533.

    Article  PubMed  PubMed Central  Google Scholar 

  • Haraldsson, M., K. Tönnesson, P. Tiselius, T. F. Thingstad & D. L. Aksnes, 2012. Relationship between fish and jellyfish as a function of eutrophication and water clarity. Marine Ecology Progress Series 471: 73–85.

    Article  Google Scholar 

  • Hays, G. C., T. K. Doyle & J. D. R. Houghton, 2018. A paradigm shift in the trophic importance of jellyfish? Trends in Ecology and Evolution 33(11): 874–884.

    Article  PubMed  Google Scholar 

  • Henschke, N., J. D. Everett, A. J. Richardson & I. M. Suthers, 2016. Rethinking the role of salps in the ocean. Trends in Ecology and Evolution 31(9): 720–733.

    Article  PubMed  Google Scholar 

  • Henschke, N., E. A. Pakhomov, L. E. Kwong, J. D. Everett, L. Laiolo, A. M. Coghlan & I. M. Suthers, 2019. Large vertical migrations of Pyrosoma atlanticum play an important role in active carbon transport. Journal of Geophysical Research: Biogeosciences 124: 1056–1070.

    Article  Google Scholar 

  • Hirst, A. G. & C. H. Lucas, 1998. Salinity influences body weight quantification in the scyphomedusa Aurelia aurita: Important implications for body weight determination in gelatinous zooplankton. Marine Ecology Progress Series 165: 259–269.

    Article  CAS  Google Scholar 

  • Iguchi, N. & T. Ikeda, 2004. Metabolism and elemental composition of aggregate and solitary forms of Salpa thompsoni (Tunicata: Thaliacea) in waters off the Antarctic Peninsula during austral summer 1999. Journal of Plankton Research 26(9): 1025–1037.

    Article  CAS  Google Scholar 

  • Iguchi, N., H. Iwatani, K. Sugimoto, S. Kitajima, N. Honda & O. Katoh, 2017. Biomass, body elemental composition, and carbon requirement of Nemopilema nomurai (Scyphozoa: Rhizostomeae) in the southwestern Japan Sea. Plankton and Benthos Research 12(2): 104–114.

    Article  Google Scholar 

  • Ikeda, T., 1984. Sequences in metabolic rates and elemental composition (C, N, P) during the development of Euphausia superba Dana and estimated food requirements during its life span. Journal of Crustacean Biology 4(1): 273–284.

    Article  Google Scholar 

  • Ikeda, T. & A. W. Mitchell, 1982. Oxygen uptake, ammonia excretion and phosphate excretion by krill and other Antarctic zooplankton in relation to their body size and chemical composition. Marine Biology 71(3): 283–298.

    Article  Google Scholar 

  • Jankowski, T., 2000. Chemical composition and biomass parameters of a population of Craspedacusta sowerbii Lank 1880 (Cnidaria: Limnomedusa). Journal of Plankton Research 22(7): 1329–1340.

    Article  CAS  Google Scholar 

  • Kremer, P., 1976. Excretion and body composition of the ctenophore Mnemiopsis leidyi (A. Agassiz): Comparisons and consequences. In: 10th European Symposium on Marine Biology, Ostend, Belgium, 17–23 September, 2: 351–362.

  • Krishnaswami, S., M. Baskaran, S. W. Fowler & M. Heyraud, 1985. Comparative role of salps and other zooplankton in the cycling and transport of selected elements and natural radionuclides in Mediterranean waters. Biochemistry 1: 353–360.

    CAS  Google Scholar 

  • Larson, R. J., 1986. Water content, organic content, and carbon and nitrogen composition of medusae from the northeast Pacific. Journal of Experimental Marine Biology and Ecology 99(2): 107–120.

    Article  Google Scholar 

  • Le Borgne, R., 1982. Zooplankton production in the eastern tropical Atlantic Ocean: net growth efficiency and P: B in terms of carbon, nitrogen, and phosphorus. Limnology and Oceanography 27(4): 681–698.

    Article  Google Scholar 

  • Le Fur, I., R. De Wit, M. Plus, J. Oheix, V. Derolez, M. Simier, N. Malet & V. Ouisse, 2019. Re-oligotrophication trajectories of macrophyte assemblages in Mediterranean coastal lagoons based on 17-year time-series. Marine Ecology Progress Series 608: 13–32.

    Article  Google Scholar 

  • Lesniowski, T. J., M. Gambill, S. Holst, M. A. Peck, M. Algueró-Muñiz, M. Haunost, A. M. Malzahn & M. Boersma, 2015. Effects of food and CO2 on growth dynamics of polyps of two scyphozoan species (Cyanea capillata and Chrysaora hysoscella). Marine Biology 162(6): 1371–1382.

    Article  CAS  Google Scholar 

  • Lucas, C. H., 1994. Biochemical composition of Aurelia aurita in relation to age and sexual maturity. Journal of Experimental Marine Biology and Ecology 183: 179–192.

    Article  CAS  Google Scholar 

  • Lüskow, F., M. D. Galbraith, B. P. V. Hunt, R. I. Perry & E. A. Pakhomov, 2021. Gelatinous and soft-bodied zooplankton in the Northeast Pacific Ocean: organic, elemental, and energy contents. Marine Ecology Progress Series 665: 19–35.

    Article  Google Scholar 

  • Madin, L. P. & G. R. Harbison, 2001. Gelatinous zooplankton. In Steele, J., S. Thorpe & K. Turekian (eds), Encyclopedia of Ocean Sciences, Vol. 2. Academic Press, London: 1120–1130.

    Chapter  Google Scholar 

  • Malej, A., J. Faganeli & J. Pezdic, 1993. Stable isotope and biochemical fractionation in the marine pelagic food chain: the jellyfish Pelagia noctiluca and net zooplankton. Marine Biology 116(4): 565–570.

    Article  CAS  Google Scholar 

  • Malej, A., V. Turk, T. Kogovšek, T. Makovec, V. Onofrri, L. Chiaverano, T. Tinta, V. Flander-Putrle & D. Lučić, 2009. Aurelia sp. 5 (Scyphozoa) population in the Mljet Lake (the southern Adriatic): trophic interactions and link to microbial food web. Annales Series Historia Naturalis 19: 49–58.

    Google Scholar 

  • Malzahn, A. M., F. Hantzsche, K. L. Schoo, M. Boermsa & N. Aberle, 2010. Differential effects of nutrient-limited primary production on primary, secondary or tertiary consumers. Oecologia 162: 35–48.

    Article  PubMed  Google Scholar 

  • Masuzawa, T., M. Koyama & M. Terazaki, 1988. A regularity in trace element contents of marine zooplankton species. Marine Biology 97(4): 587–591.

    Article  CAS  Google Scholar 

  • McNamara, M. E., D. J. Lonsdale & R. C. Aller, 2013. Elemental composition of Mnemiopsis leidyi A. Agassiz 1865 and its implications for nutrient recycling in a Long Island estuary. Estuaries and Coasts 36: 1253–1264.

    Article  CAS  Google Scholar 

  • Meunier, C. L., A. M. Malzahn & M. Boersma, 2014. A new approach to homeostatic regulation: towards a unified view of physiological and ecological concepts. PLoS ONE 9(9): e107737.

    Article  PubMed  PubMed Central  Google Scholar 

  • Meunier, C. L., S. Alvarez-Fernandez, A. Ö. Cunha-Dupont, C. Geisen, A. M. Malzahn, M. Boersma & K. H. Wiltshire, 2018. The craving for phosphorus in heterotrophic dinoflagellates and its potential implications for biogeochemical cycles. Limnology and Oceanography 63(4): 1774–1784.

    Article  CAS  Google Scholar 

  • Parsons, T. R. & C. M. Lalli, 2002. Jellyfish population explosion: Revisiting a hypothesis of possible causes. La Mer 40: 111–121.

    Google Scholar 

  • Peňuelas, J., J. Sardans, A. Rivas-Ubach & I. A. Janssens, 2012. The human-induced imbalance between C, N and P in Earth’s life system. Global Change Biology 18(1): 3–6.

    Article  Google Scholar 

  • Plum, C., H. Hillebrand & S. Moorthi, 2020. Krill vs salps: Dominance shift from krill to salps is associated with higher dissolved N: P ratios. Scientific Reports 10: 5911.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purcell, J. E., 1991. A review of cnidarians and ctenophores feeding on competitors in the plankton. Hydrobiologia 216(217): 335–342.

    Article  Google Scholar 

  • R Core Team, 2021. A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. http://www.R-project.org/.

  • Redfield, A. C., 1934. On the proportions of organic derivatives in sea water and their relation to the composition of plankton. James Johnstone Memorial Volume. University Press of Liverpool, 176–192.

  • Richardson, A. J., A. Bakun, G. C. Hays & M. J. Gibbons, 2009. The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends in Ecology and Evolution 24(6): 312–322.

    Article  PubMed  Google Scholar 

  • Robison, B. H., 2004. Deep pelagic biology. Journal of Experimental Marine Biology and Ecology 300: 253–272.

    Article  Google Scholar 

  • Schneider, G., 1988. Chemische Zusammensetzung und Biomasseparameter der Ohrenqualle Aurelia aurita. Helgoländer Meeresuntersuchungen 42: 319–327.

    Article  Google Scholar 

  • Schoo, K. L., N. Aberle, A. M. Malzahn & M. Boersma, 2010. Does the nutrient stoichiometry of primary producers affect the secondary consumer Pleurobrachia pileus? Aquatic Ecology 44: 233–242.

    Article  CAS  Google Scholar 

  • Schoo, K. L., A. M. Malzahn, E. Kraus & M. Boersma, 2013. Increased carbon dioxide availability alters phytoplankton stoichiometry and affects carbon cycling and growth of a marine planktonic herbivore. Marine Biology 160(8): 2145–2155.

    Article  CAS  Google Scholar 

  • Shangguan, Y., P. M. Gilbert, J. Alexander, C. J. Madden & S. Murasko, 2017. Phytoplankton assemblage response to changing nutrients in Florida Bay: results of mesocosm studies. Journal of Experimental Marine Biology and Ecology 494: 38–53.

    Article  CAS  Google Scholar 

  • Sommer, U., H. Stibor, A. Katechakis, F. Sommer & T. Hansen, 2002. Pelagic food web configurations at different levels of nutrient richness and their implications for the ratio fish production:primary production. Hydrobiologia 484: 11–20.

    Article  Google Scholar 

  • Sterner, R. W. & J. J. Elser, 2002. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere, Princeton University Press, Princeton, NJ:

    Google Scholar 

  • Sterner, R. W., J. Clasen, W. Lampert & T. Weisse, 1998. Carbon:phosphorus stoichiometry and food chain production. Ecology Letters 1: 146–150.

    Article  Google Scholar 

  • Thiebot, J.-B. & J. C. McInnes, 2020. Why do marine endotherms eat gelatinous prey? ICES Journal of Marine Science 77(1): 58–71.

    Google Scholar 

  • Touratier, F., F. Carlotti & G. Gorsky, 2003. Individual growth model for the appendicularian Oikopleura dioica. Marine Ecology Progress Series 248: 141–163.

    Article  Google Scholar 

  • van de Waal, D. B., A. M. Verschoor, J. M. H. Verspagen, E. van Donk & J. Huisman, 2010. Climate-driven changes in the ecological stoichiometry of aquatic ecosystems. Frontiers in Ecology and the Environment 8(3): 145–152.

    Article  Google Scholar 

  • Vijverberg, J. & H. T. Frank, 1976. The chemical composition and energy contents of copepods and cladocerans in relation to their size. Freshwater Biology 6(4): 333–345.

    Article  CAS  Google Scholar 

  • Wright, R. M., C. Le Quéré, E. Buitenhuis, S. Pitois & M. J. Gibbons, 2021. Role of jellyfish in the plankton ecosystem revealed using a global ocean biogeochemical model. Biogeosciences 18: 1291–1320.

    Article  CAS  Google Scholar 

  • Youngbluth, M. J., P. Kremer, T. G. Bailey & C. A. Jacoby, 1988. Chemical composition, metabolic rates and feeding behavior of the midwater ctenophore Bathocyroe fosteri. Marine Biology 98(1): 87–94.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Ursula Ecker, Clemens Kozian-Fleck, and Julia Haafke for their help in the laboratory with phosphorus measurements. We also thank three anonymous reviewers for constructive comments made on an earlier version of the manuscript.

Funding

FL was supported by a Ph.D. scholarship (International Doctoral Fellowship) from the University of British Columbia. MB acknowledges support from the German Federal Ministry of Education and Research (BMBF), within the BIOWEB project, and the State Agency for Agriculture, Environment and Rural Areas Schleswig-Holstein (LLUR).

Author information

Authors and Affiliations

Authors

Contributions

FL and EAP designed the study. FL, MDG, BPVH, RIP, and EAP performed the field sampling. MB supervised the formal sample analysis. FL analysed the data and drafted the original manuscript. All authors contributed to writing the final manuscript.

Corresponding author

Correspondence to Florian Lüskow.

Ethics declarations

Conflict of interest

The authors declare they have no conflict of interests.

Additional information

Handling editor: Jörg Dutz

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lüskow, F., Galbraith, M.D., Hunt, B.P.V. et al. Gelatinous and soft-bodied zooplankton in the Northeast Pacific Ocean: Phosphorus content and potential resilience to phosphorus limitation. Hydrobiologia 849, 1543–1557 (2022). https://doi.org/10.1007/s10750-021-04758-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-021-04758-9

Keywords

Navigation