Skip to main content

The Return of Shallow Shelf Seas as Extreme Environments: Anoxia and Macrofauna Reactions in the Northern Adriatic Sea

  • Chapter
  • First Online:
Anoxia

Abstract

Anoxia is a key issue in the past and present marine ecosystems. This is because no other form of disturbance so severely affects marine communities over such extensive areas. Anoxia is also the only manifestation of human-induced disturbance that was also an important factor in ancient systems. While microorganisms may rule the Earth, it is fundamentally the macrofauna that defines marine ecosystems and provides the ecosystem services on which we rely. Recurrent or intermittent hypoxia and anoxia represent the least consistent and therefore the most extreme habitat conditions for benthic communities. The unpredictable and rapid onset of anoxia-related mortalities has hampered our ability to document and understand the reactions of benthic organisms. One approach is to experimentally recreate, on a small-scale, hypoxia and anoxia in situ. We have designed and deployed an experimental anoxia generating unit (EAGU), equipped with time-lapse camera and sensor arrays, to analyze the behaviors and mortality sequences of benthic macrofauna in the Northern Adriatic (Mediterranean Sea), a model for eutrophication-related low dissolved oxygen events. This yields information that helps evaluate the condition and status of benthic communities, including in ancient marine ecosystems.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Breitburg DL, Craig JK, Fulford RS, Rose KA, Boynton WR, Brady DC, Ciotti BJ, Diaz RJ, Friedland KD, Hagy JD III, Hart DR, Hines AH, Houde ED, Kolesar SE, Nixon SW, Rice JA, Secor DH, Targett TE (2009) Nutrient enrichment and fisheries exploitation: interactive effects on estuarine living resources and their management. Hydrobiologia 629:31–47

    Article  CAS  Google Scholar 

  • Chan F, Barth JA, Luchenco J, Kirincich A, Weeks H, Peterson WT, Menge BA (2008) Emergence of anoxia in the California large marine ecosystem. Science 319:920

    Article  PubMed  CAS  Google Scholar 

  • Cloern JE (1982) Does benthos control phytoplankton biomass in South San Francisco Bay? Mar Ecol Prog Ser 9:191–202

    Article  Google Scholar 

  • Crema R, Castelli A, Prevedelli D (1991) Long term eutrophication effects on macrofaunal communities in Northern Adriatic Sea. Mar Pollut Bull 22(1):503–508

    Article  Google Scholar 

  • Danovaro R (2003) Pollution threats in the Mediterranean Sea: An overview. Chem Ecol 19:15–32

    Google Scholar 

  • Diaz RJ (2001) Overview of hypoxia around the world. J Environ Qual 30:275–281

    Article  PubMed  CAS  Google Scholar 

  • Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioral responses of benthic macrofauna. Oceanogr Mar Biol Annu Rev 33:245–303

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Druon JN, Schrimpf W, Dobricic S, Stips A (2004) Comparative assessment of large-scale marine eutrophication: North Sea area and Adriatic Sea as case studies. Mar Ecol Prog Ser 272:1–23

    Google Scholar 

  • Faganeli J, Avcin A, Fanuko N, Malej A, Turk V, Tusnik P, Vriser B, Vukovic A (1985) Bottom layer anoxia in the central part of the Gulf of Trieste in the late summer of 1983. Mar Pollut Bull 16:75–78

    Article  CAS  Google Scholar 

  • Fedra K (1978) On the ecology of the North Adriatic Sea. Wide-range investigations on the benthos: the Gulf of Trieste. Memorie di Biogeografia Adriat 9:69–87

    Google Scholar 

  • Fedra K, Ölscher EM, Scherübel C, Stachowitsch M, Wurzian RS (1976) On the ecology of a North Adriatic benthic community: distribution, standing crop and composition of the macrobenthos. Mar Biol 38:129–145

    Article  Google Scholar 

  • Franco P, Michelato A (1992) Northern Adriatic Sea: oceanography of the basin proper and the western coastal zone. Sci Total Environ, pp 35–62 (Suppl.)

    Google Scholar 

  • Gamulin-Brida H (1967) The benthic fauna of the Adriatic Sea. Oceanogr Mar Biol Annu Rev 5:535–568

    Google Scholar 

  • Gilbert D, Rabalais NN, Diaz RJ, Zhang J (2009) Evidence for greater oxygen decline rates in the coastal ocean than in the open ocean. Biogeosciences Discuss 6:9127–9160

    Article  Google Scholar 

  • Gooday AJ, Jorissen F, Levin LA, Middelburg JJ, Naqvi SWA, Rabalais NN, Scranton M, Zhang J (2009) Historical records of coastal eutrophication-induced hypoxia. Biogeosciences Discuss 6:2567–2658

    Article  Google Scholar 

  • Gray JS, Wu RS, Or YY (2002) Effects of hypoxia and organic enrichment on the coastal marine environment. Mar Ecol Prog Ser 238:249–279

    Article  Google Scholar 

  • Hallam A (2004) Catastrophes and lesser calamities. The causes of mass extinctions. Oxford University Press, Oxford

    Google Scholar 

  • Hallam A, Wignall PB (1999) Mass extinctions and sea-level changes. Earth Sci Rev 48:217–250

    Article  Google Scholar 

  • Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE, Fujita R, Heinemann D, Lenihan HS, Madin EMP, Perry MT, Selig ER, Spalding M, Steneck R, Watson R (2008) A global map of human impact on marine ecosystems. Science 319:948–952

    Article  PubMed  CAS  Google Scholar 

  • Haselmair A, Stachowitsch M, Zuschin M, Riedel B (2010) Behaviour and mortality of benthic crustaceans in response to experimentally induced hypoxia and anoxia in situ. Mar Ecol Prog Ser 414:195–208. doi:10.3354/meps08657

    Article  CAS  Google Scholar 

  • Herman PMJ, Scholten H (1990) Can suspension-feeders stabilize estuarine ecosystems? In: Barnes M, Gibson RN (eds.) Trophic relationships in the marine environment. Proceeding of the 24th European Marine Biology Symposium. Aberdeen University Press, pp 104–116

    Google Scholar 

  • Hily C (1991) Is the activity of benthic suspension feeders a factor controlling water quality in the Bay of Brest? Mar Ecol Prog Ser 69:179–188

    Article  Google Scholar 

  • Hrs-Brenko M, Medakovic D, Labura Z, Zahtila E (1994) Bivalve recovery after a mass mortality in the autumn of 1989 in the northern Adriatic Sea. Period Biol 96(4):455–458

    Google Scholar 

  • Jenkins M (2003) Prospects for biodiversity. Science 302:1175–1177

    Article  PubMed  CAS  Google Scholar 

  • Justic D (1987) Long-term eutrophication of the Northern Adriatic Sea. Mar Pollut Bull 18:281–284

    Article  CAS  Google Scholar 

  • Justic D, Legovic T, Rottini-Sandrini L (1987) Trend in the oxygen content 1911–1984 and occurrence of benthic mortality in the northern Adriatic Sea. Estuar Coast Shelf Sci 25:435–445

    Article  CAS  Google Scholar 

  • Justic D, Rabalais NN, Turner RE (1995) Stoichiometric nutrient balance and origin of coastal eutrophication. Mar Pollut Bull 30:41–46

    Google Scholar 

  • Levin LA (2002) Oxygen minimum zone influence on the community structure of deep-sea benthos. In: Thurston RV (ed.) Proceedings of the sixth international symposium on fish physiology, toxicology, and water quality, La Paz, Mexico. U.S. Environmental Protection Agency, Ecosystems Research Division, Athens, pp 121–133

    Google Scholar 

  • Levin LA (2003) Oxygen minimum zone benthos: adaptation and community response to hypoxia. Oceanogr Mar Biol Annu Rev 41:1–45

    Google Scholar 

  • Levin LA, Ekau W, Gooday AJ, Jorissen F, Middelburg JJ, Naqvi W, Neira C, Rabalais NN, Zhang J (2009) Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences Discuss 6:3563–3654

    Article  Google Scholar 

  • Loo LO, Rosenberg R (1989) Bivalve suspension-feeding dynamics and benthic-pelagic coupling in an eutrophicated marine bay. J Exp Mar Biol Ecol 130:253–276

    Article  Google Scholar 

  • Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH, Cooke RG, Kay MC, Kidwell SM, Kirby MX, Peterson CH, Jackson JBC (2006) Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312:1806–1809

    Article  PubMed  CAS  Google Scholar 

  • Machan R, Fedra K (1975) A new towed underwater camera system for wide-range benthic surveys. Mar Biol 33:75–84

    Article  Google Scholar 

  • Malej A, Malačič V (1995) Factors affecting bottom layer oxygen depletion in the Gulf of Trieste (Adriatic Sea). Annales 7:33–42

    Google Scholar 

  • McKinney F (2007) The northern Adriatic ecosystem: deep time in a shallow sea. Columbia University Press, New York

    Google Scholar 

  • McKinney F, Hageman SJ (2006) Paleozoic to modern marine ecological shift displayed in the northern Adriatic Sea: Sedimentary Record 5:4–8

    Google Scholar 

  • Occhipinti-Ambrogi A, Favruzzo M, Savini D (2002) Multi-annual variations of macrobenthos along the Emiglia-Romagna Coast (Northern Adriatic). PSZN Mar Ecol 23:307–319

    Article  Google Scholar 

  • Officer CB, Smayda TJ, Mann R (1982) Benthic filter feeding: a natural eutrophication control. Mar Ecol Prog Ser 9:203–210

    Article  Google Scholar 

  • Orel G, Mennea B (1969) I popolamenti betonici di alcuni tipi di fondo mobile del Golfo di Trieste. Pubbl Staz Zool Napoli 37:261–276

    Google Scholar 

  • Orel G, Marocco R, Vio E, Del Piero D, Della Seta G (1987) Sedimenti e biocenosi bentoniche tra la foce del Po ed il Golfo di Trieste (Alto Adriatico). Bull Ecol 18:229–241

    Google Scholar 

  • Ott JA (1992) The Adriatic benthos: problems and perspectives. In: Columbo G, Ferrari I, Ceccherelli VU, Rossi R (eds.) Marine eutrophication and population dynamics, 25th EMBS Olsen & Olsen, Fredensborg, Denmark, pp 367–378

    Google Scholar 

  • Ott J, Fedra K (1977) Stabilizing properties of a high-biomass benthic community in a fluctuating ecosystem. Helgoländer Meeresunters 30:485–494

    Article  Google Scholar 

  • Penna N, Capelacci S, Ricci F (2004) The influence of the Po River discharge on phytoplankton Bloom dynamics along the coastline of Pesaro (Italy) in the Adriatic Sea. Mar Pollut Bull 48(3–4):321–326

    Article  PubMed  CAS  Google Scholar 

  • Rabalais NN, Turner RE (2001) Hypoxia in the Northern Gulf of Mexico: description, causes and change. Coastal and Estuarine Studies 58:1–36

    Google Scholar 

  • Rabalais NN, Turner RE, Scavia D (2002) Beyond science into policy: Gulf of Mexico hypoxia and the Mississippi River. BioScience 52:129–142

    Article  Google Scholar 

  • Rabalais NN, Turner RE, Sen Gupta BK, Boesch DF, Chapman P, Murrell MC (2007) Hypoxia in the northern Gulf of Mexico: does the science support the plan to reduce, mitigate, and control hypoxia? Estuaries Coasts 30(5):753–772

    CAS  Google Scholar 

  • Rabalais NN, Diaz RJ, Levin LA, Turner RE, Gilbert D, Zhang J (2010) Dynamics and distribution of natural and human-caused coastal hypoxia. Biogeosciences 7:585–619

    Article  CAS  Google Scholar 

  • Riedel B, Stachowitsch M, Zuschin M (2008a) Sea anemones and brittle stars: unexpected predatory interactions during induced in situ oxygen crises. Mar Biol 153:1075–1085

    Article  Google Scholar 

  • Riedel B, Zuschin M, Haselmair A, Stachowitsch M (2008b) Oxygen depletion under glass: behavioural responses of benthic macrofauna to induced anoxia in the Northern Adriatic. J Exp Mar Biol Ecol 367:17–27

    Article  Google Scholar 

  • Riedl R (1980) Marine ecology – a century of changes. PSZNI Mar Ecol 1:3–46

    Article  Google Scholar 

  • Rose NA, Janiger D, Parsons ECM, Stachowitsch M (2011) Shifting baselines in scientific publications: a case study using cetacean research. Mar Policy 35:477–482

    Article  Google Scholar 

  • Rosenberg R (2001) Marine benthic faunal succession stages and related sedimentary activity. Sciencia Mar 65(suppl 2):107–109

    Google Scholar 

  • Sala E, Knowlton N (2006) Global marine biodiversity trends. Annu Rev Environ Resour 31:93–122

    Article  Google Scholar 

  • Solan M, Cardinale BJ, Downing AL, Engelhardt KAM, Ruesink JL, Srivastava DS (2004) Extinction and ecosystem function in the marine benthos. Science 306:1177–1180

    Article  PubMed  CAS  Google Scholar 

  • Stachowitsch M (1984) Mass mortality in the Gulf of Trieste: the course of community destruction. PSZNI Mar Ecol 5(3):243–264

    Article  Google Scholar 

  • Stachowitsch M (1991) Anoxia in the Northern Adriatic Sea: rapid death, slow recovery. In: Tyson RV, Pearson TH (eds.) Modern and ancient continental shelf anoxia. Geological Society Special Publication No. 58, London, pp 119–129

    Google Scholar 

  • Stachowitsch M (1992) Benthic communities: eutrophication’s “memory mode”. In: Vollenweider RA, Marchetti R, Viviani R (eds.) Marine coastal eutrophication. Science of the Total Environment, suppl 1992, pp 1017–1028

    Google Scholar 

  • Stachowitsch M (2003) Viewpoint: research on natural marine ecosystems: a lost era. Mar Pollut Bull 46:801–805

    Article  PubMed  CAS  Google Scholar 

  • Stachowitsch M, Avcin A (1988) Eutrophication-induced modifications of benthic communities. In: Eutrophication of the Mediterranean Sea: receiving capacity and monitoring of long-term effects, vol 49. Unesco Technical Reports in Marine Science, Bologna, pp 67–80

    Google Scholar 

  • Stachowitsch M, Fuchs A (1995) Long-term changes in the benthos of the Northern Adriatic. Annales 7:7–16

    Google Scholar 

  • Stachowitsch M, Fanuko N, Richter M (1990) Mucus aggregates in the Adriatic Sea: an overview of stages and occurrences. PSZNI Mar Ecol 11(4):327–350

    Article  Google Scholar 

  • Stachowitsch M, Riedel B, Zuschin M, Machan R (2007) Oxygen depletion and benthic mortalities: the first in situ experimental approach to documenting an elusive phenomenon. Limnol Oceanogr:Methods 5:344–352

    Google Scholar 

  • Stefanon A, Boldrin A (1982) The oxygen crisis of the Northern Adriatic Sea waters in late fall 1977 and its effects on benthic communities. In: Blanchard J, Mair J, Morrison I (eds.) Diving science symposium – Proceedings 6th symposium of the Confederation Mondiale des Activites Subaquatique. Natural Environmental Research Council, London, pp 167–175

    Google Scholar 

  • Tyson RV, Pearson TH (1991) Modern and ancient continental shelf anoxia: an overview. In: Tyson RV, Pearson TH (eds.) Modern and ancient continental Shelf Anoxia, vol 58. Geological Society Special Publication, London, pp 1–24

    Google Scholar 

  • UNEP United Nations Environment Programme (2004) Geo year book 2003. GEO Section/UNEP, Nairobi

    Google Scholar 

  • Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. PNAS 105:15452–15457

    Article  PubMed  CAS  Google Scholar 

  • Vatova A (1949) La fauna bentonica dell’alto e medio Adriatico. Nova Thalassia 1(3):1–110

    Google Scholar 

  • Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JBC, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790

    Article  PubMed  CAS  Google Scholar 

  • Wu RSS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45:35–45

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Gilbert D, Gooday AJ, Levin L, Naqvi SWA, Middelburg JJ, Scranton M, Ekau W, Pena A, Dewitte B, Oguz T, Monteiro PMS, Urban E, Rabalais NN, Ittekkot V, Kemp WM, Ulloa O, Elmgren R, Escobar-Briones E, Van der Plas AK (2010) Natural and human-induced hypoxia and consequences for coastal areas: synthesis and future development. Biogeosciences 7:1443–1467

    Article  CAS  Google Scholar 

  • Zuschin M, Pervesler P (1996) Secondary hardground-communities in the Northern Gulf of Trieste, Adriatic Sea. Senckenbergiana maritima 28:53–63

    Article  Google Scholar 

  • Zuschin M, Stachowitsch M (2009) Epifauna-dominated benthic shelf assemblages: lessons from the modern Adriatic Sea. Palaios 24:211–221

    Article  Google Scholar 

  • Zuschin M, Stachowitsch M, Pervesler P, Kollmann H (1999) Structural features and taphonomic pathways of a high-biomass epifauna in the northern Gulf of Trieste, Adriatic Sea. Lethaia 32(2):299–317

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael Stachowitsch .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Stachowitsch, M., Riedel, B., Zuschin, M. (2012). The Return of Shallow Shelf Seas as Extreme Environments: Anoxia and Macrofauna Reactions in the Northern Adriatic Sea. In: Altenbach, A., Bernhard, J., Seckbach, J. (eds) Anoxia. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 21. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1896-8_19

Download citation

Publish with us

Policies and ethics