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Trophic indices for micronektonic fishes reveal their dependence on the microbial system in the North Atlantic

  • 1.

    Azam, F. et al. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257–263 (1983).

    ADS 
    Article 

    Google Scholar 

  • 2.

    Legendre, L. & Le Fèvre, J. Microbial food webs and the export of biogenic carbon in oceans. Aquat. Microb. Ecol. 9, 69–77 (1995).

    Article 

    Google Scholar 

  • 3.

    Legendre, L. & Rivkin, R. B. Planktonic food webs: Microbial hub approach. Mar. Ecol. Prog. Ser. 365, 289–309 (2008).

    ADS 
    Article 

    Google Scholar 

  • 4.

    Arístegui, J., Gasol, J. M., Duarte, C. M. & Herndl, G. J. Microbial oceanography of the dark ocean’s pelagic realm. Limnol. Oceanogr. 54, 1501–1529 (2009).

    ADS 
    Article 

    Google Scholar 

  • 5.

    Roshan, S. & DeVries, T. Efficient dissolved organic carbon production and export in the oligotrophic ocean. Nat. Commun. 8, 2036. https://doi.org/10.1038/s41467-017-02227-3 (2017).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 6.

    Pauly, D. & Christensen, V. Primary production required to sustain global fisheries. Nature 374, 255–257 (1995).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 7.

    Sarmiento, J. L. & Gruber, N. Ocean Biogeochemical Dynamics (Princeton University Press, 2006).

    Google Scholar 

  • 8.

    Armengol, L., Calbet, A., Franchy, G., Rodríguez-Santos, A. & Hernández-León, S. Planktonic food web structure and trophic transfer efficiency along a productivity gradient in the tropical and subtropical Atlantic Ocean. Sci. Rep. 9, 2044. https://doi.org/10.1038/s41598-019-38507-9 (2019).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 9.

    Hernández-León, S. et al. Large deep-sea zooplankton biomass mirrors primary production in the global ocean. Nat. Commun. 11, 6048. https://doi.org/10.1038/s41467-020-19875-7 (2020).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 10.

    Wilson, R. et al. Contribution of fish to the marine inorganic carbon cycle. Science 323, 359–362 (2009).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 11.

    Jennings, S. & van der Molen, J. Trophic levels of marine consumers from nitrogen stable isotope analysis: Estimation and uncertainty. ICES J. Mar. Sci. 72, 2289–2300 (2015).

    Article 

    Google Scholar 

  • 12.

    Jennings, S., Maxwell, T. A. D., Schratzberger, M. & Milligan, S. P. Body-size dependent temporal variations in nitrogen stable isotope ratios in food webs. Mar. Ecol. Prog. Ser. 370, 199–206 (2008).

    ADS 
    Article 

    Google Scholar 

  • 13.

    Bernal, A., Olivar, M. P., Maynou, F. & de Puelles, M. L. F. Diet and feeding strategies of mesopelagic fishes in the western Mediterranean. Prog. Oceanogr. 135, 1–17 (2015).

    ADS 
    Article 

    Google Scholar 

  • 14.

    Gutiérrez-Rodríguez, A., Décima, M., Popp, B. N. & Landry, M. R. Isotopic invisibility of protozoan trophic steps in marine food webs. Limnol. Oceanogr. 59, 1590–1598 (2014).

    ADS 
    Article 
    CAS 

    Google Scholar 

  • 15.

    Hussey, N. E. et al. Rescaling the trophic structure of marine food webs. Ecol. Lett. 17, 239–250 (2014).

    PubMed 
    Article 

    Google Scholar 

  • 16.

    Nielsen, J. M., Popp, B. N. & Winder, M. Meta-analysis of amino acid stable nitrogen isotope ratios for estimating trophic position in marine organisms. Oecologia 178, 631–642 (2015).

    ADS 
    PubMed 
    Article 

    Google Scholar 

  • 17.

    Décima, M., Landry, M. R., Bradley, C. J. & Fogel, M. L. Alanine δ15N trophic fractionation in heterotrophic protists. Limnol. Oceanogr. 62, 2308–2322 (2017).

    ADS 
    Article 
    CAS 

    Google Scholar 

  • 18.

    Décima, M. & Landry, M. Resilience of plankton trophic structure to an eddy-stimulated diatom bloom in the North Pacific Subtropical Gyre. Mar. Ecol. Prog. Ser. 643, 33–48 (2020).

    ADS 
    Article 
    CAS 

    Google Scholar 

  • 19.

    Irigoien, X. et al. Large mesopelagic fish biomass and trophic efficiency in the Open Ocean. Nat. Commun. 5, 3271. https://doi.org/10.1038/ncomms4271 (2014).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 20.

    Cherel, Y., Fontaine, C., Richard, P. & Labat, J.-P. Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnol. Oceanogr. 55, 324–332 (2010).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 21.

    Young, J. W. et al. Setting the stage for a global-scale trophic analysis of marine top predators: A multi-workshop review. Rev. Fish Biol. Fish. 25, 261–272 (2015).

    Article 

    Google Scholar 

  • 22.

    Klevjer, T. A. et al. Large scale patterns in vertical distribution and behaviour of mesopelagic scattering layers. Sci. Rep. 6, 19873. https://doi.org/10.1038/srep19873 (2016).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 23.

    Olivar, M. P. et al. Mesopelagic fishes across the tropical and equatorial Atlantic: Biogeographical and vertical patterns. Prog. Oceanogr. 151, 116–137 (2017).

    ADS 
    Article 

    Google Scholar 

  • 24.

    Eduardo, L. N. et al. Trophic ecology, habitat, and migratory behaviour of the viperfish Chauliodus sloani reveal a key mesopelagic player. Sci. Rep. 10, 20996. https://doi.org/10.1038/s41598-020-77222-8 (2020).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 25.

    Valls, M. et al. Trophic structure of mesopelagic fishes in the western Mediterranean based on stable isotopes of carbon and nitrogen. J. Mar. Syst. 138, 160–170 (2014).

    Article 

    Google Scholar 

  • 26.

    Choy, C. A., Popp, B. N., Hannides, C. C. S. & Drazen, J. C. Trophic structure and food resources of epipelagic and mesopelagic fishes in the North Pacific Subtropical Gyre ecosystem inferred from nitrogen isotopic compositions. Limnol. Oceanogr. 60, 1156–1171 (2015).

    ADS 
    Article 

    Google Scholar 

  • 27.

    Olivar, M. P., Bode, A., López-Pérez, C., Hulley, P. A. & Hernández-León, S. Trophic position of lanternfishes (Pisces: Myctophidae) of the tropical and equatorial Atlantic estimated using stable isotopes. ICES J. Mar. Sci. 76, 649–661 (2019).

    Article 

    Google Scholar 

  • 28.

    Richards, T. M., Sutton, T. T. & Wells, R. J. D. Trophic structure and sources of variation influencing the stable isotope signatures of meso- and bathypelagic micronekton fishes. Front. Mar. Sci. 7, 507992. https://doi.org/10.3389/fmars.2020.507992 (2020).

    Article 

    Google Scholar 

  • 29.

    Choy, C. A. et al. Global trophic position comparison of two dominant mesopelagic fish families (Myctophidae, Stomiidae) using amino acid nitrogen isotopic analyses. PLoS ONE 7, e50133. https://doi.org/10.1371/journal.pone.0050133 (2012).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 30.

    Wang, F. et al. Trophic interactions of mesopelagic fishes in the South China Sea illustrated by stable isotopes and fatty acids. Front. Mar. Sci. 5, 522. https://doi.org/10.3389/fmars.2018.00522 (2019).

    Article 

    Google Scholar 

  • 31.

    Czudaj, S. et al. Spatial variation in the trophic structure of micronekton assemblages from the eastern tropical North Atlantic in two regions of differing productivity and oxygen environments. Deep Sea Res. 163, 103275. https://doi.org/10.1016/j.dsr.2020.103275 (2020).

    CAS 
    Article 

    Google Scholar 

  • 32.

    FishBase. A Global Information System on Fishes (University of California, 2021).

    Google Scholar 

  • 33.

    Bligh, E. G. & Dyer, W. J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917 (1959).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 34.

    Coplen, T. B. Guidelines and recommended terms for expression of stable isotope-ratio and gas-ratio measurement results. Rapid Commun. Mass Spectrom. 25, 2538–2560 (2011).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 35.

    Chikaraishi, Y. et al. Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol. Oceanogr. Methods 7, 740–750 (2009).

    CAS 
    Article 

    Google Scholar 

  • 36.

    McCarthy, M. D., Lehman, J. & Kudela, R. Compound-specific amino acid δ15N patterns in marine algae: Tracer potential for cyanobacterial vs. eukaryotic organic nitrogen sources in the ocean. Geochim. Cosmochim. Acta 103, 104–120 (2013).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 37.

    Mompeán, C., Bode, A., Gier, E. & McCarthy, M. D. Bulk vs. aminoacid stable N isotope estimations of metabolic status and contributions of nitrogen fixation to size-fractionated zooplankton biomass in the subtropical N Atlantic. Deep Sea Res. 114, 137–148 (2016).

    Article 
    CAS 

    Google Scholar 

  • 38.

    McClelland, J. W. & Montoya, J. P. Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83, 2173–2180 (2002).

    Article 

    Google Scholar 

  • 39.

    McMahon, K. W. & McCarthy, M. D. Embracing variability in amino acid d15N fractionation: Mechanisms, implications, and applications for trophic ecology. Ecosphere 7, e01511. https://doi.org/10.1002/ecs2.1511 (2016).

    Article 

    Google Scholar 

  • 40.

    Swanson, H. K. et al. A new probabilistic method for quantifying n-dimensional ecological niches and niche overlap. Ecology 96, 318–324 (2015).

    PubMed 
    Article 

    Google Scholar 

  • 41.

    Bradley, C. J. et al. Trophic position estimates of marine teleosts using amino acid compound specific isotopic analysis. Limnol. Oceanogr. Methods 13, 476–493 (2015).

    Article 

    Google Scholar 

  • 42.

    Hammer, Ø., Harper, D. A. T. & Ryan, P. D. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 1–9 (2001).

    Google Scholar 

  • 43.

    McCarthy, M. D., Benner, R., Lee, C. & Fogel, M. L. Amino acid nitrogen isotopic fractionation patterns as indicators of heterotrophy in plankton, particulate, and dissolved organic matter. Geochim. Cosmochim. Acta 71, 4727–4744 (2007).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 44.

    Hannides, C. C. S., Popp, B. N., Choy, C. A. & Drazen, J. C. Midwater zooplankton and suspended particle dynamics in the North Pacific Subtropical Gyre: A stable isotope perspective. Limnol. Oceanogr. 58, 1931–1946 (2013).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 45.

    Gloeckler, K. et al. Stable isotope analysis of micronekton around Hawaii reveals suspended particles are an important nutritional source in the lower mesopelagic and upper bathypelagic zones. Limnol. Oceanogr. 63, 1168–1180 (2018).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 46.

    Robison, B. H. Conservation of deep pelagic biodiversity. Conserv. Biol. 23, 847–858 (2009).

    PubMed 
    Article 

    Google Scholar 

  • 47.

    Brun, P. et al. Climate change has altered zooplankton-fuelled carbon export in the North Atlantic. Nat. Ecol. Evol. 3, 416–423 (2019).

    PubMed 
    Article 

    Google Scholar 

  • 48.

    Bode, M. et al. Feeding strategies of tropical and subtropical calanoid copepods throughout the eastern Atlantic Ocean: Latitudinal and bathymetric aspects. Prog. Oceanogr. 138, 268–282 (2015).

    ADS 
    Article 

    Google Scholar 

  • 49.

    Herndl, G. J. et al. Contribution of Archaea to total prokarytic production in the deep Atlantic Ocean. Appl. Environ. Microbiol. 71, 2303–2309 (2005).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 50.

    Varela, M. M., van Aken, H. M., Sintes, E., Reinthaler, T. & Herndl, G. J. Contribution of Crenarchaeota and bacteria to autotrophy in the North Atlantic interior. Environ. Microbiol. 13, 1524–1533 (2011).

    PubMed 
    Article 

    Google Scholar 

  • 51.

    Clifford, E. L. et al. Taurine is a major carbon and energy source for marine prokaryotes in the North Atlantic Ocean off the Iberian Peninsula. Microb. Ecol. 78, 299–312 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 52.

    Hoen, D. K. et al. Amino acid 15N trophic enrichment factors of four large carnivorous fishes. J. Exp. Mar. Biol. Ecol. 453, 76–83 (2014).

    CAS 
    Article 

    Google Scholar 

  • 53.

    McMahon, K. W. & McCarthy, M. D. Embracing variability in amino acid δ15N fractionation: Mechanisms, implications, and applications for trophic ecology. Ecosphere 7, e01511. https://doi.org/10.1002/ecs2.1511 (2016).

    Article 

    Google Scholar 

  • 54.

    Pauly, D., Christensen, V. & Walters, C. Ecopath, ecosim, and ecospace as tools for evaluating ecosystem impact of fisheries. ICES J. Mar. Sci. 57, 697–706 (2000).

    Article 

    Google Scholar 

  • 55.

    Christensen, V. & Walters, C. Ecopath with ecosim: Methods, capabilities and limitations. Ecol. Model. 172, 109–139 (2004).

    Article 

    Google Scholar 

  • 56.

    McClain-Counts, J. P., Demopoulos, A. W. J. & Ross, S. W. Trophic structure of mesopelagic fishes in the Gulf of Mexico revealed by gut content and stable isotope analyses. Mar. Ecol. 38, e12449. https://doi.org/10.1111/maec.12449 (2017).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 57.

    Olivar, M. P. et al. The contribution of migratory mesopelagic fishes to neuston fish assemblages across the Atlantic, Indian and Pacific Oceans. Mar. Freshw. Res. 67, 1114–1127 (2016).

    Article 

    Google Scholar 

  • 58.

    Gartner, J. V. & Musick, J. A. Feeding habits of the deep-sea fish, Scopelogadus beanii (Pisces: Melamphaide), in the western North Atlantic. Deep Sea Res. A Oceanogr. Res. Pap. 36(10), 1457–1469. https://doi.org/10.1016/0198-0149(89)90051-4 (1989).

    ADS 
    Article 

    Google Scholar 

  • 59.

    Clarke, L. J., Trebilco, R., Walters, A., Polanowski, A. M. & Deagle, B. E. DNA-based diet analysis of mesopelagic fish from the southern Kerguelen axis. Deep-Sea Res. II Top. Stud. Oceanogr. https://doi.org/10.1016/j.dsr2.2018.09.001 (2020).

    Article 

    Google Scholar 

  • 60.

    Schmoker, C., Hernández-León, S. & Calbet, A. Microzooplankton grazing in the oceans: Impacts, data variability, knowledge gaps and future directions. J. Plankton Res. 35, 691–706 (2013).

    Article 

    Google Scholar 

  • 61.

    Calbet, A. & Saiz, E. The ciliate-copepod link in marine ecosystems. Aquat. Microb. Ecol. 38, 157–167 (2005).

    Article 

    Google Scholar 

  • 62.

    Zeldis, J. R. & Décima, M. Mesozooplankton connect the microbial food web to higher trophic levels and vertical export in the New Zealand subtropical convergence zone. Deep Sea Res. 155, 103146 (2020).

    CAS 
    Article 

    Google Scholar 

  • 63.

    Jennings, S., Pinnegar, J. K., Polunin, N. V. C. & Boon, T. W. Weak cross-species relationships between body size and trophic level belie powerful size-based trophic structuring in fish communities. J. Anim. Ecol. 70, 934–944 (2001).

    Article 

    Google Scholar 

  • 64.

    Bode, A., Carrera, P. & Lens, S. The pelagic foodweb in the upwelling ecosystem of Galicia (NW Spain) during spring: Natural abundance of stable carbon and nitrogen isotopes. ICES J. Mar. Sci. 60, 11–22 (2003).

    CAS 
    Article 

    Google Scholar 

  • 65.

    Hunt, B. P. V. et al. A coupled stable isotope-size spectrum approach to understanding pelagic food-web dynamics: A case study from the southwest sub-tropical Pacific. Deep Sea Res. 113, 208–224 (2015).

    CAS 
    Article 

    Google Scholar 

  • 66.

    Romero-Romero, S., Molina-Ramírez, A., Höfer, J. & Acuña, J. L. Body size-based trophic structure of a deep marine ecosystem. Ecology 97, 171–181 (2016).

    PubMed 
    Article 

    Google Scholar 

  • 67.

    Barnes, C., Maxwell, D., Reuman, D. C. & Jennings, S. Global patterns in predator-prey size relationships reveal size dependency of trophic transfer efficiency. Ecology 91, 222–232 (2010).

    PubMed 
    Article 

    Google Scholar 

  • 68.

    Schoener, T. W. Food webs from the small to the large. Ecology 70, 1559–1589 (1989).

    Article 

    Google Scholar 

  • 69.

    Zhou, M. What determines the slope of a plankton biomass spectrum?. J. Plankton Res. 28, 437–448 (2006).

    Article 

    Google Scholar 

  • 70.

    Van der Zanden, M. J. & Fetzer, W. Global patterns of aquatic food chain length. Oikos 116, 1378–1388 (2007).

    Article 

    Google Scholar 

  • 71.

    Basedow, S. L., de Silva, N. A. L., Bode, A. & van Beusekorn, J. Trophic positions of mesozooplankton across the North Atlantic: estimates derived from biovolume spectrum theories and stable isotope analyses. J. Plankton Res. 38, 1364–1378 (2016).

    CAS 

    Google Scholar 

  • 72.

    Williams, R. J. & Martinez, N. D. Limits to trophic levels and omnivory in complex food webs: Theory and data. Am. Nat. 163, 458–468 (2004).

    PubMed 
    Article 

    Google Scholar 

  • 73.

    Nagata, T. et al. Emerging concepts on microbial processes in the bathypelagic ocean – ecology, biogeochemistry, and genomics. Deep Sea Res. II 57, 1519–1536 (2010).

    ADS 
    CAS 
    Article 

    Google Scholar 


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