SpringerLink
Log in

Biomass Pyramids of Marine Mesozooplankton Communities as Inferred From Their Integrated Trophic Positions

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Biomass pyramids in natural food webs provide insights into multitrophic ecosystem functioning. We measured the integrated trophic position (iTP), which reflects the average efficiency of biomass transfer through trophic pathways, of 14 mesozooplankton communities in the western North Pacific. Compound-specific nitrogen isotope analysis of amino acids for composite mesozooplankton biomass indicated that the iTP values of marine mesozooplankton communities and their biomass pyramids are essentially controlled by biodiversity, body weight, and species turnover. Offshore communities with lower diversity and higher iTP were dominated by large copepods with slow turnover, such as Neocalanus, whereas nearshore communities with higher diversity and lower iTP were characterized by several smaller, fast turnover species belonging to Calanus, Paracalanidae, Eucalanidae, and Metridinidae. The observed iTP values (2.36 ± 0.32) indicate different topologies in biomass pyramids in different sites, where inverted pyramids are found in less diverse communities. The results also suggest that iTP can be linked to food chain length (FCL), a conventional proxy for the biomass pyramid. Combining iTP and FCL in the future studies will be a powerful approach to better understand factors controlling food web structure and dynamics.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

Data Availability

The data that support the findings of this study are available in the electronic supplementary material (ESM) of this article.

References

  • Arim M, Abades SR, Laufer G, Loureiro M, Marquet PA. 2010. Food web structure and body size: trophic position and resource acquisition. Oikos 119:147–153.

    Article  Google Scholar 

  • Basedow SL, De Silva NA, Bode A, Van Beusekorn J. 2016. Trophic positions of mesozooplankton across the North Atlantic: estimates derived from biovolume spectrum theories and stable isotope analyses. J Plankton Res 38:1364–1378.

    CAS  Google Scholar 

  • Bonhommeau S, Dubroca L, Le Pape O, Barde J, Kaplan DM, Chassot E, Nieblas A-E. 2013. Eating up the world’s food web and the human trophic level. Proc Natl Acad Sci USA 110:20617–20620.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chikaraishi Y, Kashiyama Y, Ogawa NO, Kitazato H, Ohkouchi N. 2007. Biosynthetic and metabolic controls of nitrogen isotopic composition of amino acids in marine macroalgae and gastropods: implications for aquatic food web studies. Mar Ecol Prog Ser 342:85–90.

    Article  CAS  Google Scholar 

  • Chikaraishi Y, Ogawa NO, Kashiyama Y, Takano Y, Suga H, Tomitani A, Miyashita H, Kitazato H, Ohkouchi N. 2009. Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol Oceanogr Methods 7:740–750.

    Article  CAS  Google Scholar 

  • Chikaraishi Y, Ogawa NO, Doi H, Ohkouchi N. 2011. 15N/14N ratios of amino acids as a tool for studying terrestrial food webs: a case study of terrestrial insects (bees, wasps, and hornets). Ecol Res 26:835–844.

    Article  Google Scholar 

  • Dagg M. 1993. Sinking particles as a possible source of nutrition for the large calanoid copepod Neocalanus cristatus in the subarctic Pacific Ocean. Deep Sea Res I 40:1431–1445.

    Article  Google Scholar 

  • Décima M, Landry MR, Bradley CJ, Fogel ML. 2017. Alanine δ15N trophic fractionation in heterotrophic protists. Limnol Oceanogr 62:2308–2322.

    Article  Google Scholar 

  • Elton CS. 1927. Animal ecology. Chicago: University of Chicago Press.

    Google Scholar 

  • Garcia HE, Weathers K, Paver CR, Smolyar I, Boyer TP, Locarnini RA, Zweng MM, Mishonov AV, Baranova OK, Seidov D, Reagan JR (2018) World Ocean Atlas 2018, Volume 4: Dissolved Inorganic Nutrients (phosphate, nitrate and nitrate+nitrite, silicate). A Mishonov Technical Ed, NOAA Atlas NESDIS 84, 35pp

  • Gutiérrez-Rodríguez A, Décima M, Popp BN, Landry MR. 2014. Isotopic invisibility of protozoan trophic steps in marine food webs. Limnol Oceanogr 59:1590–1598.

    Article  Google Scholar 

  • Hannides CCS, Popp BN, Landry MR, Graham BS. 2009. Quantification of zooplankton trophic position in the North Pacific subtropical Gyre using stable nitrogen isotopes. Limnol Oceanogr 54:50–61.

    Article  CAS  Google Scholar 

  • Harrison PJ, Whitney FA, Tsuda A, Saito H, Tadokoro K. 2004. Nutrient and plankton dynamics in the NE and NW gyres of the subarctic Pacific Ocean. J Oceanogr 60:93–117.

    Article  CAS  Google Scholar 

  • Hatton IA, McCann KS, Fryxell JM, Davies TJ, Smerlak M, Sinclair AR, Loreau M. 2015. The predator–prey power law: biomass scaling across terrestrial and aquatic biomes. Science 349:aac6284.

    Article  PubMed  Google Scholar 

  • Higashi M, Burns TP, Patten BC. 1989. Food Network unfolding: an extension of trophic dynamics for application to natural ecosystems. J Theor Biol 140:243–261.

    Article  Google Scholar 

  • Hirai J, Tachibana A, Tsuda A. 2020. Large-scale metabarcoding analysis of epipelagic and mesopelagic copepods in the Pacific. PLoS ONE 15:e0233189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirata T, Hardman-Mountford NJ, Brewin RJW, Aiken J, Barlow R, Suzuki K, Isada T, Howell E, Hashioka T, Noguchi-Aita M, Yamanaka Y. 2011. Synoptic relationships between surface chlorophyll-a and diagnostic pigments specific to phytoplankton functional types. Biogeosciences 8:311–327.

    Article  CAS  Google Scholar 

  • Ikeda T, Shiga N, Yamaguchi A. 2008. Structure, biomass distribution and trophodynamics of the pelagic ecosystem in the Oyashio region, western subarctic Pacific. J Oceanogr 64:339–354.

    Article  Google Scholar 

  • Ishikawa NF. 2018. Use of compound-specific nitrogen isotope analysis of amino acids in trophic ecology: assumptions, applications, and implications. Ecol Res 33:825–837.

    Article  CAS  Google Scholar 

  • Ishikawa NF, Chikaraishi Y, Ohkouchi N, Murakami AR, Tayasu I, Togashi H, Okano J, Sakai Y, Iwata T, Kondoh M, Okuda N. 2017. Integrated trophic position decreases in more diverse communities of stream food webs. Sci Rep 7:2130.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ishikawa NF, Ogawa NO, Chikaraishi Y, Yamaguchi MO, Fujikura K, Miyairi Y, Yokoyama Y, Nagata T, Ohkouchi N. 2021. Influences of ocean currents on the diets of demersal fish communities in the western North Pacific revealed by their muscle carbon and nitrogen isotopic compositions. Front Mar Sci 8:641282.

    Article  Google Scholar 

  • Kato Y, Kondoh M, Ishikawa NF, Togashi H, Kohmatsu Y, Yoshimura M, Yoshimizu C, Haraguchi TF, Osada Y, Ohte N, Tokuchi N, Okuda N, Miki T, Tayasu I. 2018. Using food network unfolding to evaluate food-web complexity in terms of biodiversity: theory and applications. Ecol Lett 21:1065–1074.

    Article  PubMed  Google Scholar 

  • Kiørboe T. 2011. How zooplankton feed: mechanisms, traits and trade-offs. Biol Rev 86:311–339.

    Article  PubMed  Google Scholar 

  • Kobari T, Ikeda T. 1999. Vertical distribution, population structure and life cycle of Neocalanus cristatus (Crustacea: Copepoda) in the Oyashio region, with notes on its regional variations. Mar Biol 134:683–696.

    Article  Google Scholar 

  • Landry MR, Gifford DJ, Kirchman DL, Wheeler PA, Monger BC. 1993. Direct and indirect effects of grazing by Neocalanus plumchrus on plankton community dynamics in the subarctic Pacific. Prog Oceanogr 32:239–258.

    Article  Google Scholar 

  • Layman CA, Winemiller KO, Arrington DA, Jepsen DB. 2005. Body size and trophic position in a diverse tropical food web. Ecology 86:2530–2535.

    Article  Google Scholar 

  • Liang D, Uye S. 1996. Population dynamics and production of the planktonic copepods in a eutrophic inlet of the Inland Sea of Japan. II1. Paracalanus sp. Mar Biol 127:219–227.

    Article  Google Scholar 

  • Lindeman RL. 1942. The trophic-dynamic aspect of ecology. Ecology 23:399–417.

    Article  Google Scholar 

  • Locarnini RA, Mishonov AV, Baranova OK, Boyer TP, Zweng MM, Garcia HE, Reagan JR, Seidov D, Weathers K, Paver CR, Smolyar I (2018) World Ocean Atlas 2018, Volume 1: Temperature. A Mishonov Technical Ed. NOAA Atlas NESDIS 81, 52pp

  • Matsubayashi J, Osada Y, Tadokoro K, Abe Y, Yamaguchi A, Shirai K, Honda K, Yoshikawa C, Ogawa NO, Ohkouchi N, Ishikawa NF, Nagata T, Miyamoto H, Nishino S, Tayasu I. 2020. Tracking long-distance migration of marine fishes using compound-specific stable isotope analysis of amino acids. Ecol Lett 23:881–890.

    Article  PubMed  Google Scholar 

  • McCarthy MD, Benner R, Lee C, Fogel ML. 2007. Amino acid nitrogen isotopic fractionation patterns as indicators of heterotrophy in plankton, particulate, and dissolved organic matter. Geochim Cosmochim Acta 71:4727–4744.

    Article  CAS  Google Scholar 

  • McGowan JA, Walker PW. 1979. Structure in the copepod community of the North Pacific central gyre. Ecol Monogr 49:195–226.

    Article  Google Scholar 

  • Miyaguchi H, Fujiki T, Kikuchi T, Kuwahara VS, Toda T. 2006. Relationship between the bloom of Noctiluca scintillans and environmental factors in the coastal waters of Sagami Bay, Japan. J Plankton Res 28:313–324.

    Article  CAS  Google Scholar 

  • Motoda S. 1959. Devices of simple plankton apparatus. Mem Fac Fish Hokkaido Univ 7:73–94.

    Google Scholar 

  • Nagasawa S, Marumo R. 1972. Feeding of a pelagic chaetognath, Sagitta nagae Alvariño in Suruga Bay, Central Japan. J Ocean Soc Jpn 28:181–186.

    Article  Google Scholar 

  • NOAA National Geophysical Data Center (2006) 2-minute gridded global relief data (ETOPO2) v2. NOAA National Centers for Environmental Information. https://doi.org/10.7289/V5J1012Q. Accessed 7 April 2021

  • Odate T. 1994. Plankton abundance and size structure in the northern North Pacific Ocean in early summer. Fish Oceanogr 3:267–278.

    Article  Google Scholar 

  • Ogawa NO, Chikaraishi Y, Ohkouchi N. 2013. Trophic position estimates of formalin-fixed samples with nitrogen isotopic compositions of amino acids: an application to gobiid fish (Isaza) in Lake Biwa, Japan. Ecol Res 28:697–702.

    Article  Google Scholar 

  • Pauly D, Christensen V. 1995. Primary production required to sustain global fisheries. Nature 374:255–257.

    Article  CAS  Google Scholar 

  • Pauly D, Christensen V, Dalsgaard J, Froese R, Torres F. 1998. Fishing down marine food webs. Science 279:860–863.

    Article  CAS  PubMed  Google Scholar 

  • Pielou EC. 1966. Shannon’s formula as a measure of specific diversity: its use and misuse. Am Nat 100:463–465.

    Article  Google Scholar 

  • Popp BN, Graham BS, Olson RJ, Hannides CCS, Lott MJ, López-Ibarra G, others. 2007. Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids. In: Dawson TE, Siegwolf RTW, Eds. Stable isotopes as indicators of ecological change, . Amsterdam: Elsevier. pp 173–190.

    Google Scholar 

  • Purcell JE. 1981. Dietary composition and diel feeding patterns of epipelagic siphonophores. Mar Biol 65:83–90.

    Article  Google Scholar 

  • R Development Core Team. 2019. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  • Sathyendranath S, Jackson T, Brockmann C, Brotas V, Calton B, Chuprin A, Clements O, Cipollini P, Danne O, Dingle J, Donlon C, Grant M, Groom S, Krasemann H, Lavender S, Mazeran C, Mélin F, Moore TS, Müller D, Regner P, Steinmetz F, Steele C, Swinton J, Valente A, Zühlke M, Feldman G, Franz B, Frouin R, Werdell J, Platt T (2020) ESA ocean colour climate change initiative (Ocean_Colour_cci): Global chlorophyll-a data products gridded on a sinusoidal projection, Version 4.2. Centre for Environmental Data Analysis. https://catalogue.ceda.ac.uk/uuid/99348189bd33459cbd597a58c30d8d10. Accessed 7 April 2021

  • Shannon CE, Weaver W. 1963. The mathematical theory of communication. Urbana: University of Illinois Press.

    Google Scholar 

  • Takahashi K, Kuwata A, Saito H, Ide K. 2008. Grazing impact of the copepod community in the Oyashio region of the western subarctic Pacific Ocean. Prog Oceanogr 78:222–240.

    Article  Google Scholar 

  • Tsuda A, Saito H, Kasai H. 1999. Life histories of Neocalanus flemingeri and Neocalanus plumchrus (Calanoida: Copepoda) in the western subarctic Pacific. Mar Biol 135:533–544.

    Article  Google Scholar 

  • Tunney TD, McCann KS, Lester NP, Shuter BJ. 2012. Food web expansion and contraction in response to changing environmental conditions. Nat Commun 3:1105.

    Article  PubMed  Google Scholar 

  • Ward CL, McCann KS. 2017. A mechanistic theory for aquatic food chain length. Nat Commun 8:2028.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilhm JL. 1968. Use of biomass units in Shannon’s formula. Ecology 49:153–156.

    Article  Google Scholar 

  • Yokouchi K, Takeshi K, Matsumoto I, Fujiwara G, Kawamura H, Okuda K. 2000. OCTS-derived chlorophyll-a concentration and oceanic structure in the Kuroshio frontal region off the Joban/Kashima Coast of Japan. Remote Sens Environ 78:188–197.

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Haruko Umeda for identifying mesozooplankton species and screening the literature for feeding guilds; Yoko Sasaki for hel** with the laboratory work; Takeshi Okunishi for data input; Prima Anugerahanti, Sherwood Lan Smith, and Michio Kondoh for fruitful discussions; and Chisato Yoshikawa for valuable comments on the manuscript. Comments and suggestions from Martin Lindegren and an anonymous reviewer are greatly appreciated. We would also like to thank Enago for the English language review. This study was supported by the Japan Science and Technology Agency CREST (Grant Number JPMJCR13A4) and the Japan Society for the Promotion of Science Grants-in-Aid for Scientific Research (18H02513). We declare no conflict of interest.

Author information

Author notes

  1. NFI and JM designed the study. KT prepared the samples. NFI analyzed the data and wrote the first draft. All authors participated in discussions to finalize the manuscript.

Authors and Affiliations

  1. Biogeochemistry Research Center, Japan Agency for Marine-Earth Science and Technology, Yokosuka, 237-0061, Japan

    Naoto F. Ishikawa & Naohiko Ohkouchi

  2. Fisheries Resources Institute, Japan Fisheries Research and Education Agency, Shiogama, 985-0001, Japan

    Kazuaki Tadokoro

  3. Japan Fisheries Research and Education Agency, Yokohama, 236-8648, Japan

    Jun Matsubayashi

Authors
  1. Naoto F. Ishikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kazuaki Tadokoro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jun Matsubayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Naohiko Ohkouchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Naoto F. Ishikawa.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ishikawa, N.F., Tadokoro, K., Matsubayashi, J. et al. Biomass Pyramids of Marine Mesozooplankton Communities as Inferred From Their Integrated Trophic Positions. Ecosystems 26, 217–231 (2023). https://doi.org/10.1007/s10021-022-00753-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-022-00753-w

Keywords

Search

Navigation