The deep sea (>200 m depth) encompasses >95% of the world’s ocean volume and represents the largest and least explored biome on Earth (<0.0001% of ocean surface), yet is increasingly under threat from multiple direct and indirect anthropogenic pressures. Our ability to preserve both benthic and pelagic deep-sea ecosystems depends upon effective ecosystem-based management strategies and monitoring based on widely agreed deep-sea ecological variables. Here, we identify a set of deep-sea essential ecological variables among five scientific areas of the deep ocean: (1) biodiversity; (2) ecosystem functions; (3) impacts and risk assessment; (4) climate change, adaptation and evolution; and (5) ecosystem conservation. Conducting an expert elicitation (1,155 deep-sea scientists consulted and 112 respondents), our analysis indicates a wide consensus amongst deep-sea experts that monitoring should prioritize large organisms (that is, macro- and megafauna) living in deep waters and in benthic habitats, whereas monitoring of ecosystem functioning should focus on trophic structure and biomass production. Habitat degradation and recovery rates are identified as crucial features for monitoring deep-sea ecosystem health, while global climate change will likely shift bathymetric distributions and cause local extinction in deep-sea species. Finally, deep-sea conservation efforts should focus primarily on vulnerable marine ecosystems and habitat-forming species. Deep-sea observation efforts that prioritize these variables will help to support the implementation of effective management strategies on a global scale.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Scientific Reports Open Access 18 September 2023
Communications Chemistry Open Access 11 September 2023
Journal of Big Data Open Access 24 March 2023
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Rent or buy this article
Prices vary by article type
Prices may be subject to local taxes which are calculated during checkout
The dataset generated and analysed during the current study is available from the corresponding author on reasonable request.
Ramirez-Llodra, E. et al. Man and the last great wilderness: human impact on the deep sea. PLoS ONE 6, e22588 (2011).
Mengerink, K. J. et al. A call for deep-ocean stewardship. Science 344, 696–698 (2014).
Cordes, E. E. et al. Environmental impacts of the deep-water oil and gas industry: a review to guide management strategies. Front. Env. Sci. 4, 58 (2016).
Danovaro, R., Dell’Anno, A. & Pusceddu, A. Biodiversity response to climate change in a warm deep sea. Ecol. Lett. 7, 821–828 (2004).
Halpern, B. S., Selkoe, K. A., Micheli, F. & Kappel, C. V. Evaluating and ranking the vulnerability of global marine ecosystems to anthropogenic threats. Conserv. Biol. 21, 1301–1315 (2007).
Armstrong, C. W., Foley, N. S., Tinch, R. & van den Hove, S. Services from the deep: steps towards valuation of deep-sea goods and services. Ecosyst. Serv. 2, 2–13 (2012).
Thurber, A. R. et al. Ecosystem function and services provided by the deep sea. Biogeosciences 11, 3941–3963 (2014).
Danovaro, R. et al. Exponential decline of deep-sea ecosystem functioning linked to benthic biodiversity loss. Curr. Biol. 18, 1–8 (2008).
Pusceddu, A. et al. Chronic and intensive bottom trawling impairs deep-sea biodiversity and ecosystem functioning. Proc. Natl Acad. Sci. USA 111, 8861–8866 (2014).
Mora, C. et al. Biotic and human vulnerability to projected changes in ocean biogeochemistry over the 21st century. PLoS Biol. 11, e1001682 (2013).
Levin, L. & Le Bris, N. The deep ocean under climate change. Science 350, 766–768 (2015).
Sweetman, A. K. et al. Major impacts of climate change on deep-sea benthic ecosystems. Elem. Sci. Anth. 5, 4 (2017).
Hughes, T. P., Bellwood, D. R., Folke, C. S., McCook, L. J. & Pandolfi, J. M. No-take areas, herbivory and coral reef resilience. Trends Ecol. Evol. 22, 1–3 (2007).
Kachelriess, D., Wegmann, M., Gollock, M. & Pettorelli, N. The application of remote sensing for marine protected area management. Ecol. Indic. 36, 169–177 (2014).
Levin, L. A. & Dayton, P. K. Ecological theory and continental margins: where shallow meets deep. Trends Ecol. Evol. 24, 606–617 (2009).
Canals, M. et al. Flushing submarine canyons. Nature 444, 354–357 (2006).
Rogers, A. D. Environmental change in the deep ocean. Annu. Rev. Environ. Resour. 40, 1–38 (2015).
Thomsen, L. et al. The oceanic biological pump: rapid carbon transfer to depth at continental margins during winter. Sci. Rep. 7, 10763 (2017).
Scholes, R. J. et al. Building a global observing system for biodiversity. Curr. Opin. Environ. Sustain. 4, 139 (2012).
Pereira, H. M. et al. Essential biodiversity variables. Science 339, 277–278 (2013).
Lindstrom, E. J., Gunn, A., Fischer, A. & McCurdy, L. K. A Framework for Ocean Observing. By the Task Team for an Integrated Framework for Sustained Ocean Observing (UNESCO, 2012).
Levin, L. A. et al. Global observing needs in the deep ocean. Front. Mar. Sci. 6, 241 (2019).
Woodall, L. C. et al. A multidisciplinary approach for generating globally consistent data on mesophotic, deep-pelagic, and bathyal biological communities. Oceanography 31, 76–89 (2018).
Danovaro, R. et al. An ecosystem-based deep-ocean strategy. Science 355, 452–454 (2017).
Qualtrics, I. (Qualtrics, 2013).
Danovaro, R., Snelgrove, P. V. & Tyler, P. Challenging the paradigms of deep-sea ecology. Trends Ecol. Evol. 29, 465–475 (2014).
Karl, D. M. & Lukas, R. The Hawaii Ocean Time-series (HOT) program: background, rationale and field implementation. Deep-Sea Res. II 43, 129–156 (1996).
Hurtt, G. C. & Armstrong, R. A. A pelagic ecosystem model calibrated with BATS data. Deep-Sea Res. II 43, 653–683 (1996).
Aguzzi, J. & Company, J. B. Chronobiology of deep-water decapod crustaceans on continental margins. Adv. Mar. Biol. 58, 155–225 (2010).
Herná, S. et al. Carbon sequestration and zooplankton lunar cycles: could we be missing a major component of the biological pump? Limnol. Oceanogr. 55, 2503–2512 (2010).
Appeltans, W. et al. The magnitude of global marine species diversity. Curr. Biol. 22, 2189–2202 (2012).
Gotelli, N. J. & Colwell, R. K. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4, 379–391 (2001).
Yool, A. et al. Big in the benthos: future change of seafloor community biomass in a global, body size‐resolved model. Glob. Change Biol. 23, 3554–3566 (2017).
Smith, C. R., De Leo, F. C., Bernardino, A. F., Sweetman, A. K. & Arbizu, P. M. Abyssal food limitation, ecosystem structure and climate change. Trends Ecol. Evol. 23, 518–528 (2008).
Pusceddu, A., Dell’Anno, A., Fabiano, M. & Danovaro, R. Quantity and bioavailability of sediment organic matter as signatures of benthic trophic status. Mar. Ecol. Prog. Ser. 375, 41–52 (2009).
Van Dover, C. L. Hydrothermal vent ecosystems and conservation. Oceanography 25, 313–316 (2012).
Levin, L. A. et al. Hydrothermal vents and methane seeps: rethinking the sphere of influence. Front. Mar. Sci. 3, 72 (2016).
Rex, M. A. et al. Global bathymetric patterns of standing stock and body size in the deep-sea benthos. Mar. Ecol. Prog. Ser. 317, 1–8 (2006).
Danovaro, R., Corinaldesi, C., Rastelli, E. & Dell’Anno, A. Towards a better quantitative assessment of the relevance of deep-sea viruses, Bacteria and Archaea in the functioning of the ocean seafloor. Aquat. Microb. Ecol. 75, 81–90 (2015).
Gambi, C., Pusceddu, A., Benedetti‐Cecchi, L. & Danovaro, R. Species richness, species turnover and functional diversity in nematodes of the deep Mediterranean Sea: searching for drivers at different spatial scales. Glob. Ecol. Biogeogr. 23, 24–39 (2014).
Robison, B. H. Conservation of deep pelagic biodiversity. Conserv. Biol. 23, 847–858 (2009).
Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a Framework for Community Action in the field of Marine Environmental Policy (Marine Strategy Framework Directive, 2008).
Van Dover, C. L. et al. Ecological restoration in the deep sea: Desiderata. Mar. Policy 44, 98–106 (2014).
Gollner, S. et al. Resilience of benthic deep-sea fauna to mining activities. Mar. Environ. Res. 129, 76–101 (2017).
Jamieson, A. J., Malkocs, T., Piertney, S. B., Fujii, T. & Zhang, Z. Bioaccumulation of persistent organic pollutants in the deepest ocean fauna. Nat. Ecol. Evol. 1, 0051 (2017).
Morato, T., Watson, R., Pitcher, T. J. & Pauly, D. Fishing down the deep. Fish Fish. 7, 24–34 (2006).
André, M. et al. Listening to the deep: live monitoring of ocean noise and cetacean acoustic signals. Mar. Pollut. Bull. 63, 18–26 (2011).
Costello, M. J. & Chaudhary, C. Marine biodiversity, biogeography, deep-sea gradients, and conservation. Curr. Biol. 27, R511–R527 (2017).
Meier, D. V. et al. Niche partitioning of diverse sulfur-oxidizing bacteria at hydrothermal vents. ISME J. 11, 1545–1558 (2017).
Foster, L. C., Schmidt, D. N., Thomas, E., Arndt, S. & Ridgwell, A. Surviving rapid climate change in the deep sea during the Paleogene hyperthermals. Proc. Natl Acad. Sci. USA 110, 9273–9276 (2013).
Fabry, V. J., Seibel, B. A., Feely, R. A. & Orr, J. C. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Sci. 65, 414–432 (2008).
Roberts, J. M. & Cairns, S. D. Cold-water corals in a changing ocean. Curr. Opin. Environ. Sustain. 7, 118–126 (2014).
Cartes, J. E., Maynou, F., Fanelli, E., López-Pérez, C. & Papiol, V. Changes in deep-sea fish and crustacean communities at 1000–2200 m in the Western Mediterranean after 25 years: relation to hydro-climatic conditions. J. Mar. Syst. 143, 138–153 (2015).
Perry, A. L., Low, P. J., Ellis, J. R. & Reynolds, J. D. Climate change and distribution shifts in marine fishes. Science 308, 1912–1915 (2005).
Smith, K. E. & Thatje, S. The secret to successful deep-sea invasion: does low temperature hold the key? PLoS ONE 7, e51219 (2012).
Yasuhara, M., Cronin, T. M., Okahashi, H. & Linsley, B. K. Abrupt climate change and collapse of deep-sea ecosystems. Proc. Natl Acad. Sci. USA 105, 1556–1560 (2008).
Adams, D. K. et al. Surface-generated mesoscale eddies transport deep-sea products from hydrothermal vents. Science 332, 580–583 (2011).
Costello, M. J. et al. A census of marine biodiversity knowledge, resources, and future challenges. PLoS ONE 5, e12110 (2010).
Van der Grient, J. M. & Rogers, A. D. Body size versus depth: regional and taxonomical variation in deep-sea meio-and macrofaunal organisms. Adv. Mar. Biol. 71, 71–108 (2015).
Galil, B. S., Danovaro, R., Rothman, S. B. S., Gevili, R. & Goren, M. Invasive biota in the deep-sea Mediterranean: an emerging issue in marine conservation and management. Biol. Invas. 20, 281–288 (2019).
Roberts, C. M. et al. Marine reserves can mitigate and promote adaptation to climate change. Proc. Natl Acad. Sci. USA 114, 6167–6175 (2017).
Wedding, L. M. et al. From principles to practice: a spatial approach to systematic conservation planning in the deep sea. Proc. R. Soc. Lond. B 280, 20131684 (2013).
Badgley, C. et al. Biodiversity and topographic complexity: modern and geohistorical perspectives. Trends Ecol. Evol. 32, 211–226 (2017).
Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).
Brooks, T. M. et al. Global biodiversity conservation priorities. Science 313, 58–61 (2006).
Baco, A. R. et al. A synthesis of genetic connectivity in deep-sea fauna and implications for marine reserve design. Mol. Ecol. 25, 3276–3298 (2016).
Pikitch, E. K. et al. Ecosystem-based fishery management. Science 305, 346–347 (2004).
Salinas-de-León, P. et al. Deep-sea hydrothermal vents as natural egg-case incubators at the Galapagos Rift. Sci. Rep. 8, 1788 (2018).
Roberts, C. M. Deep impact: the rising toll of fishing in the deep sea. Trends Ecol. Evol. 17, 242–245 (2002).
Clark, M. R. & Dunn, M. R. Spatial management of deep-sea seamount fisheries: balancing sustainable exploitation and habitat conservation. Environ. Conserv. 39, 204–214 (2012).
Pellerin, B. A. et al. Emerging tools for continuous nutrient monitoring networks: sensors advancing science and water resources protection. J. Am. Water Resour. Assoc. 52, 993–1008 (2016).
Rochman, C. M., Cook, A. M. & Koelmans, A. A. Plastic debris and policy: using current scientific understanding to invoke positive change. Environ. Toxicol. Chem. 35, 1617–1626 (2016).
Miloslavich, P. et al. Essential ocean variables for global sustained observations of biodiversity and ecosystem changes. Glob. Change Biol. 24, 2416–2433 (2018).
Bojinski, S. et al. The concept of essential climate variables in support of climate research, applications, and policy. Bull. Am. Meteor. Soc. 95, 1431–1443 (2014).
Aguzzi, J. et al. Faunal activity rhythms influencing early community succession of an implanted whale carcass offshore in Sagami Bay, Japan. Sci. Rep. 8, 11163 (2018).
Aguzzi, J. et al. New high-tech flexible networks for the monitoring of deep-sea ecosystems. Environ. Sci. Tech. 53, 6616–6631 (2019).
Brandt, A. et al. Cutting the umbilical: new technological perspectives in benthic deep-sea research. J. Mar. Sci. Eng. 4, 36 (2016).
Steinacher, M. et al. Projected 21st century decrease in marine productivity: a multi-model analysis. Biogeosciences 7, 979–1005 (2010).
Billett, D. S. M. et al. Long-term change in the megabenthos of the Porcupine Abyssal Plain (NE Atlantic). Prog. Oceanogr. 50, 325–348 (2001).
Ruhl, H. A. & Smith, K. L. Jr Shifts in deep-sea community structure linked to climate and food supply. Science 305, 513–515 (2004).
Smith, K. L., Ruhl, H. A., Kahru, M., Huffard, C. L. & Sherman, A. D. Deep ocean communities impacted by changing climate over 24 y in the abyssal northeast Pacific Ocean. Proc. Natl Acad. Sci. USA 110, 19838–19841 (2013).
Ramirez-Llodra, E. Fecundity and life-history strategies in marine invertebrates. Adv. Mar. Biol. 43, 88–170 (2002).
McClain, C. R., Allen, A. P., Tittensor, D. P. & Rex, M. A. Energetics of life on the deep seafloor. Proc. Natl Acad. Sci. USA 109, 15366–15371 (2012).
Yasuhara, M. & Danovaro, R. Temperature impacts on deep‐sea biodiversity. Biol. Rev. 1, 275–287 (2016).
McClain, C. R. & Barry, J. P. Habitat heterogeneity, disturbance, and productivity work in concert to regulate biodiversity in deep submarine canyons. Ecology 91, 964–976 (2010).
Breitburg, D. et al. Declining oxygen in the global ocean and coastal waters. Science 359, eaam7240 (2018).
Hoegh-Guldberg, O. & Bruno, J. F. The impact of climate change on the world’s marine ecosystems. Science 328, 1523–1528 (2010).
Jones, D. O. B. et al. Biological responses to disturbance from simulated deep-sea polymetallic nodule mining. PLoS ONE 12, e0171750 (2017).
Millennium Ecosystem Assessment Ecosystems and Human Well-being: Desertification Synthesis (World Resources Institute, 2005).
Hein, L. & De Ridder, N. Desertification in the Sahel: a reinterpretation. Glob. Change Biol. 12, 751–758 (2006).
Norse, E. A. et al. Sustainability of deep-sea fisheries. Mar. Policy 36, 307–320 (2012).
Pham, C. K. et al. Deep-water longline fishing has reduced impact on Vulnerable Marine Ecosystems. Sci. Rep. 4, 4837 (2014).
Puig, P. et al. Ploughing the deep seafloor. Nature 489, 286–289 (2012).
Chiba, S. et al. Human footprint in the abyss: 30 year records of deep-sea plastic debris. Mar. Policy 96, 204–212 (2018).
Courtene-Jones, W., Quinn, B., Gary, S. F., Mogg, A. O. M. & Narayanaswamy, B. E. Microplastic pollution identified in deep-sea water and ingested by benthic invertebrates in the Rockall Trough, North Atlantic Ocean. Environ. Pollut. 231, 271–280 (2017).
Hestetun, J. T., Pomponi, S. A. & Rapp, H. T. The cladorhizid fauna (Porifera, Poecilosclerida) of the Caribbean and adjacent waters. Zootaxa 4175, 521–538 (2016).
Constable, A. J. et al. Developing priority variables (“ecosystem Essential Ocean Variables”—eEOVs) for observing dynamics and change in Southern Ocean ecosystems. J. Mar. Syst. 161, 26–41 (2016).
McIntyre, A. (ed.) Life in the World’s Oceans: Diversity, Distribution, and Abundance (John Wiley & Sons, 2010).
Danovaro, R. et al. Deep-sea biodiversity in the Mediterranean Sea: the known, the unknown, and the unknowable. PLoS ONE 5, e11832 (2010).
Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G. & Worm, B. How many species are there on Earth and in the ocean? PLoS Biol. 9, e1001127 (2011).
Gambi, C. et al. Functional response to food limitation can reduce the impact of global change in the deep‐sea benthos. Glob. Ecol. Biogeogr. 26, 1008–1021 (2017).
Holt, E. A. & Miller, S. W. Bioindicators: using organisms to measure environmental impacts. Nat. Educ. 3, 8 (2010).
Pinsky, M. L., Worm, B., Fogarty, M. J., Sarmiento, J. L. & Levin, S. A. Marine taxa track local climate velocities. Science 341, 1239–1242 (2013).
Sunday, J. M. et al. Species traits and climate velocity explain geographic range shifts in an ocean‐warming hotspot. Ecol. Lett. 18, 944–953 (2015).
Levin, L. A. & Sibuet, M. Understanding continental margin biodiversity: a new imperative. Ann. Rev. Mar. Sci. 4, 79–112 (2012).
Fanelli, E., Bianchelli, S. & Danovaro, R. Deep-sea mobile megafauna of Mediterranean submarine canyons and open slopes: analysis of spatial and bathymetric gradients. Progr. Oceanogr. 168, 23–34 (2018).
Dunn, D. C. et al. A strategy for the conservation of biodiversity on mid-ocean ridges from deep-sea mining. Sci. Adv. 4, eaar4313 (2018).
FAO Vulnerable Marine Ecosystems Database (FAO, March 2019); https://go.nature.com/2uBsfOC
Miller, K. A., Thompson, K. F., Johnston, P. & Santillo, D. An overview of seabed mining including the current state of development, environmental impacts, and knowledge gaps. Front. Mar. Sci. 4, 418 (2018).
Rogers, A. D., Clark, M. R., Hall-Spencer, J. M. & Gjerde, K. M. The Science Behind the Guidelines: A Scientific Guide to the FAO Draft International Guidelines (December 2007) for the Management of Deep-Sea Fisheries in the High Seas and Examples of how the Guidelines may be Practically Implemented (IUCN, 2008).
We deeply thank M. Rex (University of Massachusetts) for valuable discussion and suggestions on an early draft of the manuscript. We are very grateful to M. Baker for supporting the authors in the distribution of the Qualtrics survey to the INDEEP and DOSI communities and to the deep-sea scientists that participated to the survey and J. Cerri for the analysis of Qualtrics results. This work was supported by the H2020 project MERCES (GA N. 689518) and IDEM (GA N. 11.0661/2017/750680/SUB/EN V.C2.). E.R.-L. was supported by the Norwegian project MarMine (247626), the Norwegian Institute for Water Research and the H2020 project MERCES (GA N. 689518). P.V.R.S. was supported by the NSERC Canadian Healthy Oceans Network and CFREF Ocean Frontier Institute. L.T. is supported by JPI Oceans2 and ONC. J.A. is supported by ARIM (Autonomous Robotic sea-floor Infrastructure for bentho-pelagic Monitoring; MartTERA ERA-Net Cofound). L.L. acknowledges NSF grant OCE 1634172 and the Deep-Ocean Observing Strategy subcontract from the Consortium for Ocean Leadership. H.R. was supported by the EMSO-Link project of the European Commission (Grant agreement ID: 731036).
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Ranking of the essential variables for biodiversity measures. Results of the Expert Elicitation obtained by using the Plackett–Luce model for the analysis about the prioritization of essential variables for biodiversity measures (y axis). The worth of each variable is reported on log scale (x axis). Average weighted Cohen’s κ is also reported on the upper part of the graph. ES, expected species number.
Ranking of the readiness of the available technologies for deep-sea ecological monitoring. Results of the Plackett–Luce model for the analysis of responses about the readiness of technology for deep-sea monitoring according to the essential variables identified for each scientific area. The Cohen’s κ value is reported on the upper part of each graph.
About this article
Cite this article
Danovaro, R., Fanelli, E., Aguzzi, J. et al. Ecological variables for developing a global deep-ocean monitoring and conservation strategy. Nat Ecol Evol 4, 181–192 (2020). https://doi.org/10.1038/s41559-019-1091-z
This article is cited by
Journal of Big Data (2023)
Scientific Reports (2023)
Communications Chemistry (2023)
International Journal of Computer Vision (2023)
Factors affecting the availability of data on East African wildlife: the monitoring needs of conservationists are not being met
Biodiversity and Conservation (2023)