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Annual Review of Marine Science

Volume 16, 2024

Life in the Midwater: The Ecology of Deep Pelagic Animals

Abstract

The water column of the deep ocean is dark, cold, low in food, and under crushing pressures, yet it is full of diverse life. Due to its enormous volume, this mesopelagic zone is home to some of the most abundant animals on the planet. Rather than struggling to survive, they thrive—owing to a broad set of adaptations for feeding, behavior, and physiology. Our understanding of these adaptations is constrained by the tools available for exploring the deep sea, but this tool kit is expanding along with technological advances. Each time we apply a new method to the depths, we gain surprising insights about genetics, ecology, behavior, physiology, diversity, and the dynamics of change. These discoveries show structure within the seemingly uniform habitat, limits to the seemingly inexhaustible resources, and vulnerability in the seemingly impervious environment. To understand midwater ecology, we need to reimagine the rules that govern terrestrial ecosystems. By spending more time at depth—with whatever tools are available—we can fill the knowledge gaps and better link ecology to the environment throughout the water column.

Keyword(s): biodiversity, deep-sea ecosystems, extreme environments, fishes, food-web ecology, mesopelagic, methodology, plankton
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/content/journals/10.1146/annurev-marine-031623-095435
2024-01-17
2024-04-27
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Literature Cited

  1. Allan EA, DiBenedetto MH, Lavery AC, Govindarajan AF, Zhang WG. 2021. Modeling characterization of the vertical and temporal variability of environmental DNA in the mesopelagic ocean. Sci. Rep. 11:21273
     [Google Scholar]
  2. Alldredge AL, Silver MW. 1988. Characteristics, dynamics and significance of marine snow. Prog. Oceanogr. 20:41–82
     [Google Scholar]
  3. Amon DJ, Gollner S, Morato T, Smith CR, Chen C et al. 2022. Assessment of scientific gaps related to the effective environmental management of deep-seabed mining. Mar. Policy 138:105006
     [Google Scholar]
  4. Angel MV. 1989. Vertical profiles of pelagic communities in the vicinity of the Azores Front and their implications to deep ocean ecology. Prog. Oceanogr. 22:1–46
     [Google Scholar]
  5. Angel MV. 1993. Biodiversity of the pelagic ocean. Conserv. Biol. 7:760–72
     [Google Scholar]
  6. Baldwin Fergus JL, Johnsen S, Osborn KJ. 2015. A unique apposition compound eye in the mesopelagic hyperiid amphipod Paraphronima gracilis. Curr. Biol. 25:473–78
     [Google Scholar]
  7. Båmstedt U, Kaartvedt S, Youngbluth M. 2003. An evaluation of acoustic and video methods to estimate the abundance and vertical distribution of jellyfish. J. Plankton Res. 25:1307–18
     [Google Scholar]
  8. Bandara K, Varpe Ø, Wijewardene L, Tverberg V, Eiane K. 2021. Two hundred years of zooplankton vertical migration research. Biol. Rev. 96:1547–89
     [Google Scholar]
  9. Benoit-Bird KJ, Au WWL, Brainard RE, Lammers MO. 2001. Diel horizontal migration of the Hawaiian mesopelagic boundary community observed acoustically. Mar. Ecol. Prog. Ser. 217:1–14
     [Google Scholar]
  10. Benoit-Bird KJ, Moline MA. 2021. Vertical migration timing illuminates the importance of visual and nonvisual predation pressure in the mesopelagic zone. Limnol. Oceanogr. 66:3010–19
     [Google Scholar]
  11. Berkenpas EJ, Henning BS, Shepard CM, Turchik AJ, Robinson CJ et al. 2018. A buoyancy-controlled lagrangian camera platform for in situ imaging of marine organisms in midwater scattering layers. IEEE J. Ocean. Eng. 43:595–607
     [Google Scholar]
  12. Bessho-Uehara M, Mallefet J, Haddock SHD 2023. Glowing sea cucumbers: bioluminescence in Holothuroidea. The World of Sea Cucumbers: Challenges, Advances, and Innovations A Mercier, J-F Hamel, A Suhrbier, C Pearce San Diego, CA: Academic. In press
     [Google Scholar]
  13. Boyd PW, Bach LT, Hurd CL, Paine E, Raven JA, Tamsitt V. 2022. Potential negative effects of ocean afforestation on offshore ecosystems. Nat. Ecol. Evol. 6:675–83
     [Google Scholar]
  14. Bracken-Grissom HD, DeLeo DM, Porter ML, Iwanicki T, Sickles J, Frank TM. 2020. Light organ photosensitivity in deep-sea shrimp may suggest a novel role in counterillumination. Sci. Rep. 10:4485
     [Google Scholar]
  15. Braun CD, Arostegui MC, Thorrold SR, Papastamatiou YP, Gaube P et al. 2022. The functional and ecological significance of deep diving by large marine predators. Annu. Rev. Mar. Sci. 14:129–59
     [Google Scholar]
  16. Breitburg D, Levin LA, Oschlies A, Grégoire M, Chavez FP et al. 2018. Declining oxygen in the global ocean and coastal waters. Science 359:eaam7240
     [Google Scholar]
  17. Carleton KL, Escobar-Camacho D, Stieb SM, Cortesi F, Marshall NJ. 2020. Seeing the rainbow: mechanisms underlying spectral sensitivity in teleost fishes. J. Exp. Biol. 223:jeb193334
     [Google Scholar]
  18. Charette MA, Smith WHF. 2010. The volume of Earth's ocean. Oceanography 23:2112–14
     [Google Scholar]
  19. Chen RS, Portner EJ, Choy CA. 2022. Gelatinous cephalopods as important prey for a deep-sea fish predator. Mar. Biol. 169:155
     [Google Scholar]
  20. Childress JJ. 1995. Are there physiological and biochemical adaptations of metabolism in deep-sea animals?. Trees 10:30–36
     [Google Scholar]
  21. Childress JJ, Barnes AT, Quetin LB, Robison BH. 1978. Thermally protecting cod ends for the recovery of living deep-sea animals. Deep-Sea Res. I 25:419–22
     [Google Scholar]
  22. Childress JJ, Price MH. 1983. Growth rate of the bathypelagic crustacean Gnathophausia ingens (Mysidacea: Lophogastridae). Mar. Biol. 76:165–77
     [Google Scholar]
  23. Childress JJ, Seibel BA. 1998. Life at stable low oxygen levels: adaptations of animals to oceanic oxygen minimum layers. J. Exp. Biol. 201:1223–32
     [Google Scholar]
  24. Childress JJ, Thuesen EV 1992. Metabolic potential of deep-sea animals: regional and global scales. Deep-Sea Food Chains and the Global Carbon Cycle GT Rowe, V Pariente 217–36. Dordrecht, Neth.: Kluwer Acad.
     [Google Scholar]
  25. Choy CA, Drazen JC. 2013. Plastic for dinner? Observations of frequent debris ingestion by pelagic predatory fishes from the central North Pacific. Mar. Ecol. Prog. Ser. 485:155–63
     [Google Scholar]
  26. Choy CA, Haddock SHD, Robison BH. 2017. Deep pelagic food web structure as revealed by in situ feeding observations. Proc. R. Soc. B 284:20172116
     [Google Scholar]
  27. Choy CA, Popp BN, Hannides CCS, Drazen JC. 2015. Trophic structure and food resources of epipelagic and mesopelagic fishes in the North Pacific Subtropical Gyre ecosystem inferred from nitrogen isotopic compositions. Limnol. Oceanogr. 60:1156–71
     [Google Scholar]
  28. Choy CA, Portner E, Iwane M, Drazen JC. 2013. Diets of five important predatory mesopelagic fishes of the central North Pacific. Mar. Ecol. Prog. Ser. 492:169–84
     [Google Scholar]
  29. Choy CA, Robison BH, Gagne TO, Erwin B, Firl E et al. 2019. The vertical distribution and biological transport of marine microplastics across the epipelagic and mesopelagic water column. Sci. Rep. 9:7843
     [Google Scholar]
  30. Choy CA, Wabnitz CCC, Weijerman M, Woodworth-Jefcoats PA, Polovina JJ. 2016. Finding the way to the top: how the composition of oceanic mid-trophic micronekton groups determines apex predator biomass in the central North Pacific. Mar. Ecol. Prog. Ser. 549:9–25
     [Google Scholar]
  31. Christianson LM, Johnson SB, Schultz DT, Haddock SHD. 2022. Hidden diversity of Ctenophora revealed by new mitochondrial COI primers and sequences. Mol. Ecol. Resour. 22:283–94
     [Google Scholar]
  32. Clarke GL, Backus RH. 1956. Measurements of light penetration in relation to vertical migration and records of luminescence of deep-sea animals. Deep-Sea Res. I 4:1–14
     [Google Scholar]
  33. Clarke TA. 1980. Diets of fourteen species of vertically migrating mesopelagic fishes in Hawaiian waters. Fish. Bull. 78:619–40
     [Google Scholar]
  34. Cook AB, Bernard AM, Boswell KM, Bracken-Grissom H, D'Elia M et al. 2020. A multidisciplinary approach to investigate deep-pelagic ecosystem dynamics in the Gulf of Mexico following Deepwater Horizon. Front. Mar. Sci. 7:548880
     [Google Scholar]
  35. Cowen RK, Guigand CM. 2008. In situ Ichthyoplankton Imaging System (ISIIS): system design and preliminary results. Limnol. Oceanogr. Methods 6:126–32
     [Google Scholar]
  36. Cronin TW. 2016. Camouflage: being invisible in the open ocean. Curr. Biol. 26:R1179–81
     [Google Scholar]
  37. Dachs J, Lohmann R, Ockenden WA, Méjanelle L, Eisenreich SJ, Jones KC. 2002. Oceanic biogeochemical controls on global dynamics of persistent organic pollutants. Environ. Sci. Technol. 36:4229–37
     [Google Scholar]
  38. Damian-Serrano A, Haddock SHD, Dunn CW. 2021. The evolution of siphonophore tentilla for specialized prey capture in the open ocean. PNAS 118:e2005063118
     [Google Scholar]
  39. Damian-Serrano A, Hetherington ED, Choy CA, Haddock SHD, Lapides A, Dunn CW. 2022. Characterizing the secret diets of siphonophores (Cnidaria: Hydrozoa) using DNA metabarcoding. PLOS ONE 17:e0267761
     [Google Scholar]
  40. de Busserolles F, Fogg L, Cortesi F, Marshall J. 2020. The exceptional diversity of visual adaptations in deep-sea teleost fishes. Semin. Cell Dev. Biol. 106:20–30
     [Google Scholar]
  41. Dischereit A, Wangensteen OS, Præbel K, Auel H, Havermans C. 2022. Using DNA metabarcoding to characterize the prey spectrum of two co-occurring Themisto amphipods in the rapidly changing Atlantic-Arctic gateway Fram Strait. Genes 13:2035
     [Google Scholar]
  42. Djurhuus A, Closek CJ, Kelly RP, Pitz KJ, Michisaki RP et al. 2020. Environmental DNA reveals seasonal shifts and potential interactions in a marine community. Nat. Commun. 11:254
     [Google Scholar]
  43. Douglas RH, Partridge JC. 1997. On the visual pigments of deep-sea fish. J. Fish Biol. 50:68–85
     [Google Scholar]
  44. Drazen JC, Popp BN, Choy CA, Clemente T, Forest LD, Smith KL Jr. 2008. Bypassing the abyssal benthic food web: macrourid diet in the eastern North Pacific inferred from stomach content and stable isotopes analyses. Limnol. Oceanogr. 53:2644–54
     [Google Scholar]
  45. Drazen JC, Smith CR, Gjerde KM, Haddock SHD, Carter GS et al. 2020. Midwater ecosystems must be considered when evaluating environmental risks of deep-sea mining. PNAS 117:17455–60
     [Google Scholar]
  46. Drazen JC, Sutton TT. 2017. Dining in the deep: the feeding ecology of deep-sea fishes. Annu. Rev. Mar. Sci. 9:337–66
     [Google Scholar]
  47. Duffy LM, Kuhnert PM, Pethybridge HR, Young JW, Olson RJ et al. 2017. Global trophic ecology of yellowfin, bigeye, and albacore tunas: understanding predation on micronekton communities at ocean-basin scales. Deep-Sea Res. II 140:55–73
     [Google Scholar]
  48. Durkin CA, Buesseler KO, Cetinić I, Estapa ML, Kelly RP, Omand M. 2021. A visual tour of carbon export by sinking particles. Glob. Biogeochem. Cycles 35:e2021GB006985
     [Google Scholar]
  49. Friedman ST, Price SA, Corn KA, Larouche O, Martinez CM, Wainwright PC. 2020. Body shape diversification along the benthic-pelagic axis in marine fishes. Proc. R. Soc. B 287:20201053
     [Google Scholar]
  50. Gates AR, Benfield MC, Booth DJ, Fowler AM, Skropeta D, Jones DOB. 2017. Deep-sea observations at hydrocarbon drilling locations: contributions from the SERPENT Project after 120 field visits. Deep-Sea Res. II 137:463–79
     [Google Scholar]
  51. Gloeckler K, Choy CA, Hannides CCS, Close HG, Goetze E et al. 2018. 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. 63:1168–80
     [Google Scholar]
  52. Goetze E, Andrews KR, Peijnenburg KTCA, Portner E, Norton EL. 2015. Temporal stability of genetic structure in a mesopelagic copepod. PLOS ONE 10:e0136087
     [Google Scholar]
  53. Gorsky G, Picheral M, Stemmann L. 2000. Use of the Underwater Video Profiler for the study of aggregate dynamics in the North Mediterranean. Estuar. Coast. Shelf Sci. 50:121–28
     [Google Scholar]
  54. Graham BS, Grubbs D, Holland K, Popp BN. 2007. A rapid ontogenetic shift in the diet of juvenile yellowfin tuna from Hawaii. Mar. Biol. 150:647–58
     [Google Scholar]
  55. Greene CH, Widder EA, Youngbluth MJ, Tamse A, Johnson GE. 1992. The migration behavior, fine structure, and bioluminescent activity of krill sound-scattering layers. Limnol. Oceanogr. 37:650–58
     [Google Scholar]
  56. Haddock SHD, Case JF. 1999. Bioluminescence spectra of shallow and deep-sea gelatinous zooplankton: ctenophores, medusae and siphonophores. Mar. Biol. 133:571–82
     [Google Scholar]
  57. Haddock SHD, Choy CA. 2020. Treasure and turmoil in the deep sea. New York Times Aug. 14. https://www.nytimes.com/2020/08/14/opinion/deep-ocean-mining-pollution.html
    [Google Scholar]
  58. Haddock SHD, Dunn CW. 2015. Fluorescent proteins function as a prey attractant: experimental evidence from the hydromedusa Olindias formosus and other marine organisms. Biol. Open 4:1094–104
     [Google Scholar]
  59. Haddock SHD, Dunn CW, Pugh PR, Schnitzler CE. 2005. Bioluminescent and red-fluorescent lures in a deep-sea siphonophore. Science 309:263
     [Google Scholar]
  60. Haddock SHD, Moline MA, Case JF. 2010. Bioluminescence in the sea. Annu. Rev. Mar. Sci. 2:443–93
     [Google Scholar]
  61. Hamilton BM, Rochman CM, Hoellein TJ, Robison BH, Van Houtan KS, Choy CA. 2021. Prevalence of microplastics and anthropogenic debris within a deep-sea food web. Mar. Ecol. Prog. Ser. 675:23–33
     [Google Scholar]
  62. Hannides CCS, Popp BN, Choy CA, Drazen JC. 2013. Midwater zooplankton and suspended particle dynamics in the North Pacific Subtropical Gyre: a stable isotope perspective. Limnol. Oceanogr. 58:1931–46
     [Google Scholar]
  63. Hannides CCS, Popp BN, Close HG, Benitez-Nelson CR, Ka'apu-Lyons CA et al. 2020. Seasonal dynamics of midwater zooplankton and relation to particle cycling in the North Pacific Subtropical Gyre. Prog. Oceanogr. 182:102266
     [Google Scholar]
  64. Henschke N, Pakhomov EA, Kwong LE, Everett JD, Laiolo L et al. 2019. Large vertical migrations of Pyrosoma atlanticum play an important role in active carbon transport. J. Geophys. Res. Biogeosci. 124:1056–70
     [Google Scholar]
  65. Herndl GJ, Bayer B, Baltar F, Reinthaler T. 2023. Prokaryotic life in the deep ocean's water column. Annu. Rev. Mar. Sci. 15:461–83
     [Google Scholar]
  66. Herring P. 2001. The Biology of the Deep Ocean Oxford, UK: Oxford Univ. Press
  67. Hetherington ED, Choy CA, Thuesen EV, Haddock SHD. 2022a. Three distinct views of deep pelagic community composition based on complementary sampling approaches. Front. Mar. Sci. 9:864004
     [Google Scholar]
  68. Hetherington ED, Damian-Serrano A, Haddock SHD, Dunn CW, Choy CA. 2022b. Integrating siphonophores into marine food-web ecology. Limnol. Oceanogr. Lett. 7:81–95
     [Google Scholar]
  69. Hirai J, Tachibana A, Tsuda A. 2020. Large-scale metabarcoding analysis of epipelagic and mesopelagic copepods in the Pacific. PLOS ONE 15:e0233189
     [Google Scholar]
  70. Holland KN, Grubbs RD. 2008. Fish visitors to seamounts: tunas and bill fish at seamounts. Seamounts: Ecology, Fisheries and Conservation189–201. Oxford, UK: Blackwell
     [Google Scholar]
  71. Hopcroft RR, Robison BH. 1999. A new mesopelagic larvacean, Mesochordaeus erythrocephalus, sp. nov., from Monterey Bay, with a description of its filtering house. J. Plankton Res. 10:1923–37
     [Google Scholar]
  72. Hopkins TL, Baird RC. 1973. Diet of the hatchetfish Sternoptyx diaphana. Mar. Biol. 21:34–46
     [Google Scholar]
  73. Hoving HJT, Haddock SHD. 2017. The giant deep-sea octopus Haliphron atlanticus forages on gelatinous fauna. Sci. Rep. 7:44952
     [Google Scholar]
  74. Huffard CL, Durkin CA, Wilson SE, McGill PR, Henthorn R, Smith KL. 2020. Temporally-resolved mechanisms of deep-ocean particle flux and impact on the seafloor carbon cycle in the northeast Pacific. Deep-Sea Res. II 173:104763
     [Google Scholar]
  75. Jackson GD, Buxton NG, George MJA. 2000. Diet of the southern opah Lampris immaculatus on the Patagonian Shelf; the significance of the squid Moroteuthis ingens and anthropogenic plastic. Mar. Ecol. Prog. Ser. 206:261–71
     [Google Scholar]
  76. Jamieson AJ, Lindsay DJ, Kitazato H. 2023. Maximum depth extensions for Hydrozoa, Tunicata and Ctenophora. Mar. Biol. 170:33
     [Google Scholar]
  77. Jamieson AJ, Linley TD. 2021. Hydrozoans, scyphozoans, larvaceans and ctenophores observed in situ at hadal depths. J. Plankton Res. 43:20–32
     [Google Scholar]
  78. Jennings RM, Bucklin A, Pierrot-Bults A. 2010. Barcoding of arrow worms (Phylum Chaetognatha) from three oceans: genetic diversity and evolution within an enigmatic phylum. PLOS ONE 5:e9949
     [Google Scholar]
  79. Johnsen S. 2005. The red and the black: bioluminescence and the color of animals in the deep sea. Integr. Comp. Biol. 45:234–46
     [Google Scholar]
  80. Johnsen S. 2014. Hide and seek in the open sea: pelagic camouflage and visual countermeasures. Annu. Rev. Mar. Sci. 6:369–92
     [Google Scholar]
  81. Johnson SB, Winnikoff JR, Schultz DT, Christianson LM, Patry WL et al. 2022. Speciation of pelagic zooplankton: invisible boundaries can drive isolation of oceanic ctenophores. Front. Genet. 13:970314
     [Google Scholar]
  82. Kaartvedt S, Klevjer TA, Torgersen T, Sørnes TA. 2007. Diel vertical migration of individual jellyfish (Periphylla periphylla). Limnol. Oceanogr. 52:975–83
     [Google Scholar]
  83. Kaartvedt S, Staby A, Aksnes DL. 2012. Efficient trawl avoidance by mesopelagic fishes causes large underestimation of their biomass. Mar. Ecol. Prog. Ser. 456:1–6
     [Google Scholar]
  84. Kane IA, Clare MA, Miramontes E, Wogelius R, Rothwell JJ et al. 2020. Seafloor microplastic hotspots controlled by deep-sea circulation. Science 368:1140–45
     [Google Scholar]
  85. Kenitz KM, Anderson CR, Carter ML, Eggleston E, Seech K et al. 2023. Environmental and ecological drivers of harmful algal blooms revealed by automated underwater microscopy. Limnol. Oceanogr. 68:598–615
     [Google Scholar]
  86. Kharbush JJ, Close HG, Van Mooy BAS, Arnosti C, Smittenberg RH et al. 2020. Particulate organic carbon deconstructed: molecular and chemical composition of particulate organic carbon in the ocean. Front. Mar. Sci 7:518
     [Google Scholar]
  87. Kiørboe T. 2011. How zooplankton feed: mechanisms, traits and trade-offs. Biol. Rev. 86:311–39
     [Google Scholar]
  88. Klevjer TA, Torres DJ, Kaartvedt S. 2012. Distribution and diel vertical movements of mesopelagic scattering layers in the Red Sea. Mar. Biol. 159:1833–41
     [Google Scholar]
  89. Kwong LE, Pakhomov EA, Suntsov AV, Seki MP, Brodeur RD et al. 2018. An intercomparison of the taxonomic and size composition of tropical macrozooplankton and micronekton collected using three sampling gears. Deep-Sea Res. I 135:34–45
     [Google Scholar]
  90. Lam PJ, Doney SC, Bishop JKB. 2011. The dynamic ocean biological pump: insights from a global compilation of particulate organic carbon, CaCO3, and opal concentration profiles from the mesopelagic. Glob. Biogeochem. Cycles. 25:GB3009
     [Google Scholar]
  91. Law KL. 2017. Plastics in the marine environment. Annu. Rev. Mar. Sci. 9:205–29
     [Google Scholar]
  92. Levin LA. 2018. Manifestation, drivers, and emergence of open ocean deoxygenation. Annu. Rev. Mar. Sci. 10:229–60
     [Google Scholar]
  93. Levin LA, Alfaro-Lucas JM, Colaço A, Cordes EE, Craik N et al. 2023. Deep-sea impacts of climate interventions. Science 379:978–81
     [Google Scholar]
  94. Levin LA, Amon DJ, Lily H. 2020. Challenges to the sustainability of deep-seabed mining. Nat. Sustain. 3:784–94
     [Google Scholar]
  95. Longhurst AR. 2007. Ecological Geography of the Sea San Diego, CA: Academic. , 2nd ed..
  96. Looser R, Froescheis O, Cailliet GM, Jarman WM, Ballschmiter K. 2000. The deep-sea as a final global sink of semivolatile persistent organic pollutants? Part II: organochlorine pesticides in surface and deep-sea dwelling fish of the North and South Atlantic and the Monterey Bay Canyon (California). Chemosphere 40:661–70
     [Google Scholar]
  97. Luck DG, Pietsch TW. 2008. In-situ observations of a deep-sea ceratioid anglerfish of the genus Oneirodes (lophiiformes: Oneirodidae). Copeia 2008:446
     [Google Scholar]
  98. Luo T, Kramer K, Goldgof DB, Hall LO, Samson S et al. 2004. Recognizing plankton images from the shadow image particle profiling evaluation recorder. IEEE Trans. Syst. Man Cybern. B 34:1753–62
     [Google Scholar]
  99. Marlétaz F, Le Parco Y, Liu S, Peijnenburg KTCA 2017. Extreme mitogenomic variation in natural populations of chaetognaths. Genome Biol. Evol. 9:1374–84
     [Google Scholar]
  100. Martini S, Haddock SHD. 2017. Quantification of bioluminescence from the surface to the deep sea demonstrates its predominance as an ecological trait. Sci. Rep. 7:45750
     [Google Scholar]
  101. Martini S, Kuhnz L, Mallefet J, Haddock SHD. 2019. Distribution and quantification of bioluminescence as an ecological trait in the deep sea benthos. Sci. Rep. 9:14654
     [Google Scholar]
  102. Maynard SD, Riggs FV, Walters JF. 1975. Mesopelagic micronekton in Hawaiian waters: faunal composition, standing stock, and diel vertical migration. Fish. Bull. 73:726–36
     [Google Scholar]
  103. McClain CR, Schlacter TA. 2015. On some hypotheses of diversity of animal life at great depths on the sea floor. Mar. Ecol. 36:849–72
     [Google Scholar]
  104. McDonnell AMP, Lam PJ, Lamborg CH, Buesseler KO, Sanders R et al. 2015. The oceanographic toolbox for the collection of sinking and suspended marine particles. Prog. Oceanogr. 133:17–31
     [Google Scholar]
  105. Meech ME, Mills CE, Haddock SHD, Meech RW. 2021. Two swimming modes in Trachymedusae; bell kinematics and the role of giant axons. J. Exp. Biol. 224:jeb239830
     [Google Scholar]
  106. Messíe M, Sherlock RE, Huffard CL, Pennington JT, Choy CA et al. 2023. Coastal upwelling drives ecosystem temporal variability from the surface to the abyssal seafloor. PNAS 120:e2214567120
     [Google Scholar]
  107. Milligan RJ, Bernard AM, Boswell KM, Bracken-Grissom HD, D'Elia MA et al. 2018. The application of novel research technologies by the Deep Pelagic Nekton Dynamics of the Gulf of Mexico (DEEPEND) consortium. Mar. Technol. Soc. J. 52:81–86
     [Google Scholar]
  108. Miyamoto H, Machida RJ, Nishida S. 2010. Genetic diversity and cryptic speciation of the deep sea chaetognath Caecosagitta macrocephala (Fowler, 1904). Deep-Sea Res. II 57:2211–19
     [Google Scholar]
  109. Mogdans J. 2019. Sensory ecology of the fish lateral-line system: morphological and physiological adaptations for the perception of hydrodynamic stimuli. J. Fish Biol. 95:53–72
     [Google Scholar]
  110. Morato T, Watson R, Pitcher TJ, Pauly D 2006. Fishing down the deep. Fish Fish 7:24–34
     [Google Scholar]
  111. Nielsen J, Hedeholm RB, Heinemeier J, Bushnell PG, Christiansen JS et al. 2016. Eye lens radiocarbon reveals centuries of longevity in the Greenland shark (Somniosus microcephalus). Science 353:702–4
     [Google Scholar]
  112. Nonaka A, Milisen JW, Mundy BC, Johnson GD. 2021. Blackwater diving: an exciting window into the planktonic arena and its potential to enhance the quality of larval fish collections. Ichthyol. Herpetol. 109:138–56
     [Google Scholar]
  113. Norse EA, Brooke S, Cheung WWL, Clark MR, Ekeland I et al. 2012. Sustainability of deep-sea fisheries. Mar. Policy 36:307–20
     [Google Scholar]
  114. Okada S, Chen C, Watsuji T-O, Nishizawa M, Suzuki Y et al. 2019. The making of natural iron sulfide nanoparticles in a hot vent snail. PNAS 116:20376–81
     [Google Scholar]
  115. Pagès F, Corbera J, Lindsay D. 2007. Piggybacking pycnogonids and parasitic narcomedusae on Pandea rubra (Anthomedusae, Pandeidae). Plankton Benthos Res 2:83–90
     [Google Scholar]
  116. Parzanini C, Parrish CC, Hamel J-F, Mercier A. 2019. Reviews and syntheses: insights into deep-sea food webs and global environmental gradients revealed by stable isotope (δ15N, δ13C) and fatty acid trophic biomarkers. Biogeosciences 16:2837–56
     [Google Scholar]
  117. Passow U, Ziervogel K. 2016. Marine snow sedimented oil released during the Deepwater Horizon spill. Oceanography 29:3118–25
     [Google Scholar]
  118. Passow U, Ziervogel K, Asper V, Diercks A. 2012. Marine snow formation in the aftermath of the Deepwater Horizon oil spill in the Gulf of Mexico. Environ. Res. Lett. 7:035301
     [Google Scholar]
  119. Peijnenburg KTCA, Breeuwer JAJ, Pierrot-Bults AC, Menken SBJ. 2004. Phylogeography of the planktonic chaetognath Sagitta setosa reveals isolation in European seas. Evolution 58:1472–87
     [Google Scholar]
  120. Pethybridge HR, Choy CA, Polovina JJ, Fulton EA. 2018. Improving marine ecosystem models with biochemical tracers. Annu. Rev. Mar. Sci. 10:199–228
     [Google Scholar]
  121. Pitz KJ, Guo J, Johnson SB, Campbell TL, Zhang H et al. 2020. Zooplankton biogeographic boundaries in the California Current System as determined from metabarcoding. PLOS ONE 15:e0235159
     [Google Scholar]
  122. Portner EJ, Markaida U, Robinson CJ, Gilly WF. 2020. Trophic ecology of Humboldt squid, Dosidicus gigas, in conjunction with body size and climatic variability in the Gulf of California, Mexico. Limnol. Oceanogr. 65:732–48
     [Google Scholar]
  123. Portner EJ, Polovina JJ, Choy CA. 2017. Patterns in micronekton diversity across the North Pacific Subtropical Gyre observed from the diet of longnose lancetfish (Alepisaurus ferox). Deep-Sea Res. I 125:40–51
     [Google Scholar]
  124. Potier M, Marsac F, Cherel Y, Lucas V, Sabatié R et al. 2007. Forage fauna in the diet of three large pelagic fishes (lancetfish, swordfish and yellowfin tuna) in the western equatorial Indian Ocean. Fish. Res. 83:60–72
     [Google Scholar]
  125. Priede IG. 2017. Deep-Sea Fishes: Biology, Diversity, Ecology and Fisheries Cambridge, UK: Cambridge Univ. Press
  126. Priede IG, Froese R. 2013. Colonization of the deep sea by fishes. J. Fish Biol. 83:1528–50
     [Google Scholar]
  127. Proud R, Cox MJ, Brierley AS. 2017. Biogeography of the global ocean's mesopelagic zone. Curr. Biol. 27:113–19
     [Google Scholar]
  128. Pugh PR, Haddock SHD. 2016. A description of two new species of the genus Erenna (Siphonophora: Physonectae: Erennidae), with notes on recently collected specimens of other Erenna species. Zootaxa 4189:401–46
     [Google Scholar]
  129. Ralston S, Field JC, Sakuma KM. 2015. Long-term variation in a central California pelagic forage assemblage. J. Mar. Syst. 146:26–37
     [Google Scholar]
  130. Ramirez-Llodra E, Tyler PA, Baker MC, Bergstad OA, Clark MR et al. 2011. Man and the last great wilderness: human impact on the deep sea. PLOS ONE 6:e22588
     [Google Scholar]
  131. Reygondeau G, Guidi L, Beaugrand G, Henson SA, Koubbi P et al. 2018. Global biogeochemical provinces of the mesopelagic zone. J. Biogeogr. 45:500–14
     [Google Scholar]
  132. Ricart AM, Krause-Jensen D, Hancke K, Price NN, Masqué P, Duarte CM. 2022. Sinking seaweed in the deep ocean for carbon neutrality is ahead of science and beyond the ethics. Environ. Res. Lett. 17:081003
     [Google Scholar]
  133. Roark EB, Guilderson TP, Dunbar RB, Fallon SJ, Mucciarone DA. 2009. Extreme longevity in proteinaceous deep-sea corals. PNAS 106:5204–8
     [Google Scholar]
  134. Robinson C, Steinberg DK, Anderson TR, Arístegui J, Carlson CA et al. 2010. Mesopelagic zone ecology and biogeochemistry—a synthesis. Deep-Sea Res. II 57:1504–18
     [Google Scholar]
  135. Robison BH. 2004. Deep pelagic biology. J. Exp. Mar. Biol. Ecol. 300:253–72
     [Google Scholar]
  136. Robison BH. 2009. Conservation of deep pelagic biodiversity. Conserv. Biol. 23:847–58
     [Google Scholar]
  137. Robison BH, Raskoff K, Sherlock R. 2005a. Ecological substrate in midwater: Doliolula equus, a new mesopelagic tunicate. J. Mar. Biol. Assoc. UK 85:655–63
     [Google Scholar]
  138. Robison BH, Reisenbichler KR, Sherlock RE. 2005b. Giant larvacean houses: rapid carbon transport to the deep sea floor. Science 308:1609–11
     [Google Scholar]
  139. Robison BH, Reisenbichler KR, Sherlock RE. 2017. The coevolution of midwater research and ROV technology at MBARI. Oceanography 30:426–37
     [Google Scholar]
  140. Robison BH, Sherlock RE, Reisenbichler KR. 2010. The bathypelagic community of Monterey canyon. Deep-Sea Res. II 57:1551–56
     [Google Scholar]
  141. Robison BH, Sherlock RE, Reisenbichler KR, McGill PR. 2020. Running the gauntlet: assessing the threats to vertical migrators. Front. Mar. Sci 7:64
     [Google Scholar]
  142. Roe HSJ. 1988. Midwater biomass profiles over the Madeira Abyssal Plain and the contribution of copepods. Biology of Copepods GA Boxshall, HK Schminke 169–81. Dordrecht, Neth: Springer
     [Google Scholar]
  143. Romero-Romero S, Herrero L, Fernández M, Gómara B, Acuña JL. 2017. Biomagnification of persistent organic pollutants in a deep-sea, temperate food web. Sci. Total Environ. 605–6:589–97
     [Google Scholar]
  144. Rosa R, Lopes VM, Guerreiro M, Bolstad K, Xavier JC. 2017. Biology and ecology of the world's largest invertebrate, the colossal squid (Mesonychoteuthis hamiltoni): a short review. Polar Biol 40:1871–83
     [Google Scholar]
  145. Saba GK, Burd AB, Dunne JP, Hernández-León S, Martin AH et al. 2021. Toward a better understanding of fish-based contribution to ocean carbon flux. Limnol. Oceanogr. 66:1639–64
     [Google Scholar]
  146. Samerotte AL, Drazen JC, Brand GL, Seibel BA, Yancey PH. 2007. Correlation of trimethylamine oxide and habitat depth within and among species of teleost fish: an analysis of causation. Physiol. Biochem. Zool. 80:197–208
     [Google Scholar]
  147. Santoro AE, Richter RA, Dupont CL. 2019. Planktonic marine archaea. Annu. Rev. Mar. Sci. 11:131–58
     [Google Scholar]
  148. Santos RG, Machovsky-Capuska GE, Andrades R. 2021. Plastic ingestion as an evolutionary trap: toward a holistic understanding. Science 373:56–60
     [Google Scholar]
  149. Schultz DT, Haddock SHD, Bredeson JV, Green RE, Simakov O, Rokhsar DS. 2023. Ancient gene linkages support ctenophores as sister to other animals. Nature 618:110–17
     [Google Scholar]
  150. Seibel BA. 2011. Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones. J. Exp. Biol. 214:326–36
     [Google Scholar]
  151. Seibel BA, Childress JJ. 2013. The real limits to marine life: a further critique of the Respiration Index. Biogeosciences 10:2815–19
     [Google Scholar]
  152. Seibel BA, Thuesen EV, Childress JJ, Gorodezky LA. 1997. Decline in pelagic cephalopod metabolism with habitat depth reflects differences in locomotory efficiency. Biol. Bull. 192:262–78
     [Google Scholar]
  153. Seibel BA, Walsh PJ. 2001. Potential impacts of CO2 injection on deep-sea biota. Science 294:319–20
     [Google Scholar]
  154. Seibel BA, Walsh PJ. 2003. Biological impacts of deep-sea carbon dioxide injection inferred from indices of physiological performance. J. Exp. Biol. 206:641–50
     [Google Scholar]
  155. Shanks AL, Trent JD. 1980. Marine snow: sinking rates and potential role in vertical flux. Deep-Sea Res. A 27:137–43
     [Google Scholar]
  156. Sherman K. 1991. The large marine ecosystem concept: research and management strategy for living marine resources. Ecol. Appl. 1:349–60
     [Google Scholar]
  157. Simmonds JE. 2005. Fisheries Acoustics: Theory and Practice Oxford. UK: Blackwell
  158. Somero GN. 2022. The Goldilocks principle: a unifying perspective on biochemical adaptation to abiotic stressors in the sea. Annu. Rev. Mar. Sci. 14:1–23
     [Google Scholar]
  159. Sosik HM, Olson RJ. 2007. Automated taxonomic classification of phytoplankton sampled with imaging-in-flow cytometry. Limnol. Oceanogr. Methods 5:204–16
     [Google Scholar]
  160. Spitz J, Cherel Y, Bertin S, Kiszka J, Dewez A, Ridoux V. 2011. Prey preferences among the community of deep-diving odontocetes from the Bay of Biscay, Northeast Atlantic. Deep-Sea Res. I 58:273–82
     [Google Scholar]
  161. Steinberg DK, Landry MR. 2017. Zooplankton and the ocean carbon cycle. Annu. Rev. Mar. Sci. 9:413–44
     [Google Scholar]
  162. Steinberg DK, Silver MW, Pilskaln CH. 1997. Role of mesopelagic zooplankton in the community metabolism of giant larvacean house detritus in Monterey Bay, California, USA. Mar. Ecol. Prog. Ser. 147:167–79
     [Google Scholar]
  163. Steinberg DK, Stamieszkin K, Maas AE, Durkin CA, Passow U et al. 2023. The outsized role of salps in carbon export in the subarctic northeast Pacific Ocean. Glob. Biogeochem. Cycles 37:e2022GB007523
     [Google Scholar]
  164. Stühmer W. 2015. Exocytosis from chromaffin cells: hydrostatic pressure slows vesicle fusion. Philos. Trans. R. Soc. Lond. B 370:20140192
     [Google Scholar]
  165. Sutton TT. 2013. Vertical ecology of the pelagic ocean: classical patterns and new perspectives. J. Fish Biol. 83:1508–27
     [Google Scholar]
  166. Sutton TT, Clark MR, Dunn DC, Halpin PN, Rogers AD et al. 2017. A global biogeographic classification of the mesopelagic zone. Deep-Sea Res. I 126:85–102
     [Google Scholar]
  167. Sutton TT, Hopkins TL. 1996. Trophic ecology of the stomiid (Pisces: Stomiidae) fish assemblage of the eastern Gulf of Mexico: strategies, selectivity and impact of a top mesopelagic predator group. Mar. Biol. 127:179–92
     [Google Scholar]
  168. Thomas KN, Robison BH, Johnsen S. 2017. Two eyes for two purposes: in situ evidence for asymmetric vision in the cockeyed squids Histioteuthis heteropsis and Stigmatoteuthis dofleini. Philos. Trans. R. Soc. Lond. B 372:20160069
     [Google Scholar]
  169. Thuesen EV, Childress JJ. 1993. Enzymatic activities and metabolic rates of pelagic chaetognaths: lack of depth-related declines. Limnol. Oceanogr. 38:935–48
     [Google Scholar]
  170. Thuesen EV, Childress JJ. 1994. Oxygen consumption rates and metabolic enzyme activities of oceanic California medusae in relation to body size and habitat depth. Biol. Bull. 187:84–98
     [Google Scholar]
  171. Thuesen EV, Rutherford LD, Brommer PL. 2005. The role of aerobic metabolism and intragel oxygen in hypoxia tolerance of three ctenophores: Pleurobrachia bachei, Bolinopsis infundibulum and Mnemiopsis leidyi. J. Mar. Biol. Assoc. UK 85:627–33
     [Google Scholar]
  172. Toggweiler JR, Key RM 2003. Ocean circulation: thermohaline circulation. Encyclopedia of Atmospheric Sciences JR Holton, J Pyle, JA Curry 1549–55. San Diego, CA: Academic
     [Google Scholar]
  173. Torres JJ, Bailey TG. 2022. Life in the Open Ocean: The Biology of Pelagic Species Hoboken, NJ: Wiley & Sons
  174. Torres JJ, Belman WW, Childress JJ. 1979. Oxygen consumption rates of midwater fishes as a function of depth of occurrence. Deep-Sea Res. A 26:185–97
     [Google Scholar]
  175. Tsuda A, Miller CB. 1998. Mate-finding behaviour in Calanus marshallae Frost. Philos. Trans. R. Soc. Lond. B 353:713–20
     [Google Scholar]
  176. Urban P, Praebel K, Bhat S, Dierking J, Wangensteen OS. 2022. DNA metabarcoding reveals the importance of gelatinous zooplankton in the diet of Pandalus borealis, a keystone species in the Arctic. Mol. Ecol. 31:1562–76
     [Google Scholar]
  177. Uttal L, Buck KR. 1996. Dietary study of the midwater polychaete Poeobius meseres in Monterey Bay, California. Mar. Biol. 125:333–43
     [Google Scholar]
  178. van der Sluijs I, Gray SM, Amorim MCP, Barber I, Candolin U et al. 2011. Communication in troubled waters: responses of fish communication systems to changing environments. Evol. Ecol. 25:623–40
     [Google Scholar]
  179. Vinogradov ME. 1970. Vertical Distribution of the Oceanic Zooplankton, Vol. 1 Jerusalem: Isr. Program Sci. Transl.
  180. Wagner H-J. 2002. Sensory brain areas in three families of deep-sea fish (slickheads, eels and grenadiers): comparison of mesopelagic and demersal species. Mar. Biol. 141:807–17
     [Google Scholar]
  181. Wagner H-J, Douglas RH, Frank TM, Roberts NW, Partridge JC. 2009. A novel vertebrate eye using both refractive and reflective optics. Curr. Biol. 19:108–14
     [Google Scholar]
  182. Warrant EJ, Locket NA. 2004. Vision in the deep sea. Biol. Rev. 79:671–712
     [Google Scholar]
  183. Widder E, Johnsen S, Bernstein S, Case J, Neilson D. 1999. Thin layers of bioluminescent copepods found at density discontinuities in the water column. Mar. Biol. 134:429–37
     [Google Scholar]
  184. Widmer CL, Cailliet G, Geller J. 2010. The life cycle of Earleria corachloeae n. sp. (Cnidaria: Hydrozoa) with epibiotic hydroids on mid-water shrimp. Mar. Biol. 157:49–58
     [Google Scholar]
  185. Wiebe PH, Morton AW, Bradley AM, Backus RH, Craddock JE et al. 1985. New development in the MOCNESS, an apparatus for sampling zooplankton and micronekton. Mar. Biol. 87:313–23
     [Google Scholar]
  186. Wilson SE, Ruhl HA, Smith KL Jr. 2013. Zooplankton fecal pellet flux in the abyssal northeast Pacific: a 15 year time-series study. Limnol. Oceanogr. 58:881–92
     [Google Scholar]
  187. Winnikoff JR, Haddock SHD, Budin I. 2021. Depth- and temperature-specific fatty acid adaptations in ctenophores from extreme habitats. J. Exp. Biol. 224:jeb242800
     [Google Scholar]
  188. Wishner KF, Seibel BA, Roman C, Deutsch C, Outram D et al. 2018. Ocean deoxygenation and zooplankton: Very small oxygen differences matter. Sci. Adv. 4:eaau5180
     [Google Scholar]
  189. Woodall LC, Sanchez-Vidal A, Canals M, Paterson GLJ, Coppock R et al. 2014. The deep sea is a major sink for microplastic debris. R. Soc. Open Sci. 1:140317
     [Google Scholar]
  190. Woodstock MS, Zhang Y. 2022. Towards ecosystem modeling in the deep sea: a review of past efforts and primer for the future. Deep-Sea Res. I 188:103851
     [Google Scholar]
  191. Yancey PH. 2005. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208:2819–30
     [Google Scholar]
  192. Yancey PH, Fyfe-Johnson AL, Kelly RH, Walker VP, Auñón MT. 2001. Trimethylamine oxide counteracts effects of hydrostatic pressure on proteins of deep-sea teleosts. J. Exp. Zool. 289:172–76
     [Google Scholar]
  193. Yancey PH, Gerringer ME, Drazen JC, Rowden AA, Jamieson A. 2014. Marine fish may be biochemically constrained from inhabiting the deepest ocean depths. PNAS 111:4461–65
     [Google Scholar]
  194. Yen J, Lasley R. 2011. Chemical communication between copepods: finding the mate in a fluid environment. Chemical Communication in Crustaceans T Breithaupt, M Thiel 177–97. New York: Springer
     [Google Scholar]
  195. Yen J, Strickler JR. 1996. Advertisement and concealment in the plankton: What makes a copepod hydrodynamically conspicuous?. Invertebr. Biol. 115:191–205
     [Google Scholar]
  196. Yoshino K, Takahashi A, Adachi T, Costa DP, Robinson PW et al. 2020. Acceleration-triggered animal-borne videos show a dominance of fish in the diet of female northern elephant seals. J. Exp. Biol. 223:jeb212936
     [Google Scholar]
  197. Young JW, Hunt BPV, Cook TR, Llopiz JK, Hazen EL et al. 2015. The trophodynamics of marine top predators: current knowledge, recent advances and challenges. Deep-Sea Res. II 113:170–87
     [Google Scholar]
  198. Young JW, Lansdell MJ, Campbell RA, Cooper SP, Juanes F, Guest MA. 2010. Feeding ecology and niche segregation in oceanic top predators off eastern Australia. Mar. Biol. 157:2347–68
     [Google Scholar]
  199. Young RE. 1975. Function of the dimorphic eyes in the midwater squid Histioteuthis dofleini. Pac. Sci. 29:211–18
     [Google Scholar]
  200. Zhao S, Zettler ER, Bos RP, Lin P, Amaral-Zettler LA, Mincer TJ. 2022. Large quantities of small microplastics permeate the surface ocean to abyssal depths in the South Atlantic Gyre. Glob. Change Biol. 28:2991–3006
     [Google Scholar]
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Life in the Midwater: The Ecology of Deep Pelagic Animals
Annual Review of Marine Science 16, 383 (2024); https://doi.org/10.1146/annurev-marine-031623-095435
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