Oceanography The Official Magazine of
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Volume 25 Issue 03

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Volume 25, No. 3
Pages 188 - 201

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Pelagic-Benthic Coupling, Food Banks, and Climate Change on the West Antarctic Peninsula Shelf

By Craig R. Smith , David J. DeMaster, Carrie J. Thomas , Pavica Sršen , Laura Grange , Victor Evrard , and Fabio DeLeo  
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Article Abstract

The West Antarctic Peninsula (WAP) shelf is deep and detritus-based (i.e., it is fueled by organic material sinking from intense seasonal cycles of primary production in the water column), leading to pelagic-benthic coupling. The WAP is warming rapidly, yielding increases in seawater temperatures and reductions in sea ice that may fundamentally alter pelagic-benthic coupling and shelf benthic ecosystems. RVIB Nathaniel B. Palmer and ARSV Laurence M. Gould have provided year-round access to the WAP sea ice zone, facilitating studies of pelagic-benthic coupling and climate change. In the Food for Benthos along the Antarctic Continental Shelf (FOODBANCS) Project, we conducted a 15-month field program to evaluate benthic ecosystem function across the mid-WAP shelf, testing the hypothesis that “phytodetrital material deposited from the summer bloom provides a sustained source of food for benthic detritivores during winter months, when organic-matter flux from the water column is extremely low.” We found that the intense seasonality in primary production and food availability in the WAP water column is heavily dampened at the shelf floor by the presence of a “food bank” that sustains benthic ecosystem functions (including sediment-community respiration, deposit feeding, vitellogenesis, spawning, and recruitment of benthos) over the winter; this food bank also influences community structure and life-history strategies of the WAP benthos. The persistence of the food bank may be mediated by low bottom-water temperatures, with the consequence that climate warming might reduce food availability in shelf communities. During the FOODBANCS2 Project, we studied the benthic ecosystem response to the strong latitudinal sea ice gradient along the WAP to explore the ecosystem consequences of sea ice loss from climate change. We found that some aspects of benthic ecosystem structure (e.g., macrofaunal dominance by the polychaete Aurospio foodbancsia) covaried with sea ice duration and are likely to be sensitive to sea ice loss. Other benthic parameters (e.g., the standing crop of macro- and megabenthos) exhibited nonlinear responses, with evidence of resilience along much of the sea ice gradient and abrupt change near one end. Still other benthic parameters (e.g., sediment community respiration) changed very little with sea ice duration. We also found that climate warming is facilitating invasion of the WAP shelf by predacious king crabs, with dramatic reduction in benthic biodiversity and altered ecosystem function. In summary, some important benthic ecosystem parameters along the WAP may be resilient to climate-induced changes in pelagic-benthic coupling, while many others may be highly sensitive, responding nonlinearly to sea ice loss. Incorporation of climate change effects into WAP benthic ecosystem models, including the effects of invasive species, will be challenging until mechanisms, nonlinearities, synergies, and tipping points of climate change effects are better understood.

Citation

Smith, C.R., D.J. DeMaster, C. Thomas, P. Sršen, L. Grange, V. Evrard, and F. DeLeo. 2012. Pelagic-benthic coupling, food banks, and climate change on the West Antarctic Peninsula Shelf. Oceanography 25(3):188–201, https://doi.org/10.5670/oceanog.2012.94.

References
    Arnosti, C., and B.B. Jørgensen. 2003. High activity and low temperature optima of extracellular enzymes in Arctic sediments: Implications for carbon cycling by heterotrophic microbial communities. Marine Ecology Progress Series 249:15–24, https://doi.org/10.3354/meps249015.
  1. Arntz, W.E., T. Brey, and V.A. Gallardo. 1994. Antarctic zoobenthos. Pp. 241–304 in Oceanography and Marine Biology: An Annual Review, vol. 32. H. Barnes, A.D. Ansell, R.N. Gibson, and M. Barnes, eds, University College London Press.
  2. Arntz, W.E., and J.M. Gili. 2001. A case for tolerance in marine ecology: Let us not put out the baby with the bathwater. Scientia marina 65(suppl.):283–299.
  3. Aronson, R.B., S. Thatje, A. Clarke, L.S. Peck, D.B. Blake, C.D. Wilga, and B.A. Seibel. 2007. Climate change and invasibility of the Antarctic benthos. Annual Review of Ecology, Evolution, and Systematics 38:129–154, https://doi.org/10.1146/annurev.ecolsys.38.091206.095525.
  4. Atkinson, A., V. Siegel, E. Pakhomov, and P. Rothery. 2004. Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432:100–103, https://doi.org/10.1038/nature02996.
  5. Beaulieu, S.E. 2002. Accumulation and fate of phytodetritus on the sea floor. Pp. 171–232 in Oceanography and Marine Biology: An Annual Review, vol. 40. R.N. Gibson, M. Barnes, and R.J.A. Atkinson, eds, Taylor and Francis.
  6. Berkman, P.A., and S.L. Forman. 1996. Pre‐bomb radiocarbon and the reservoir correction for calcareous marine species in the Southern Ocean. Geophysical Research Letters 23(4):363–366, https://doi.org/10.1029/96GL00151.
  7. Buesseler, K.O., A.M.P. McDonnell, O.M.E. Schofield, D.K. Steinberg, and H.W. Ducklow. 2010. High particle export over the continental shelf of the west Antarctic Peninsula. Geophysical Research Letters 37, L22606, https://doi.org/10.1029/2010GL045448.
  8. Clarke, A. 1985. Food webs and interactions: An overview of the Antarctic ecosystem. Pp. 329–350 in Antarctica. W.N. Bonner and D.W.H. Walton, eds, Pergamon, Oxford, UK.
  9. Clarke, A., H.J. Griffiths, D.K.A. Barnes, M.P. Meredith, and S.M. Grant. 2009. Spatial variation in seabed temperatures in the Southern Ocean: Implications for benthic ecology and biogeography. Journal of Geophysical Research 114, G03003, https://doi.org/10.1029/2008JG000886.
  10. Clarke, A., E.J. Murphy, M.P. Meredith, J.C. King, L.S. Peck, D.K.A. Barnes, and R.C. Smith. 2007. Climate change and the marine ecosystem of the western Antarctic Peninsula. Philosophical Transactions of the Royal Society B 362:149–166, https://doi.org/10.1098/rstb.2006.1958.
  11. Cook, A.J., A.J. Fox, D.G. Vaughan, and J.G. Ferrigno. 2005. Retreating glacier fronts on the Antarctic Peninsula over the past half-century. Science 308:541–544, https://doi.org/10.1126/science.1104235.
  12. Dayton, P.K. 1990. Polar benthos. Pp. 631–685 in Polar Oceanography, Part B: Chemistry, Biology, and Geology. W.O. Smith, ed., Academic Press, London.
  13. DeMaster, D.J., C.J. Thomas, C.R. Smith, R. Pirtle-Levy, B. Pointer, A. Hopkins, K. Null, P. Sršen, and V. Evrard. 2011. FOODBANCS-2: Biogeochemical distributions and ecological processes along a N/S transect on the western Antarctic Peninsula shelf. P. 65 in ASLO 2011 Aquatic Sciences Meeting Book of Abstracts. Available online at: http://aslo.org/sanjuan2011/files.html (accessed July 12, 2012).
  14. Ding, Q., E.J. Steig, D.S. Battisti, and M. Küttel. 2011. Winter warming in West Antarctica caused by central tropical Pacific warming. Nature Geoscience 4(6):398–403, https://doi.org/10.1038/ngeo1129.
  15. Ducklow, H.W., K. Baker, D.G. Martinson, L.B. Quetin, R.M. Ross, R.C. Smith, S.E. Stammerjohn, M. Vernet, and W. Fraser. 2007. Marine pelagic ecosystems: The west Antarctic Peninsula. Philosophical Transactions of the Royal Society B 362(1477):67–94, https://doi.org/10.1098/rstb.2006.1955.
  16. Ducklow, H.W., M. Erickson, J. Kelly, M. Montes-Hugo, C.A. Ribic, R.C. Smith, S.E. Stammerjohn, and D.M. Karl. 2008. Particle export from the upper ocean over the continental shelf of the west Antarctic Peninsula: A long-term record, 1992–2007. Deep Sea Research Part II 55:2,118–2,131, https://doi.org/10.1016/j.dsr2.2008.04.028.
  17. Ducklow, H.W., W. Fraser, D.M. Karl, L.B. Quetin, R.M. Ross, R.C. Smith, S.E. Stammerjohn, M. Vernet, and R.M. Daniels. 2006. Water-column processes in the West Antarctic Peninsula and the Ross Sea: Interannual variations and foodweb structure. Deep Sea Research Part II 53:834–852, https://doi.org/10.1016/j.dsr2.2006.02.009.
  18. Galley, E.A., P.A. Tyler, A. Clarke, and C.R. Smith. 2005. Reproductive biology and biochemical composition of the brooding echinoid Amphipneustes lorioli on the Antarctic continental shelf. Marine Biology 148(1):59–71, https://doi.org/10.1007/s00227-005-0069-3.
  19. Galley, E.A., P.A. Tyler, C.R. Smith, and A. Clarke. 2008. Reproductive biology of two species of holothurian from the deep-sea order Elasipoda, on the Antarctic continental shelf. Deep Sea Research Part II 55:2,515–2,526, https://doi.org/10.1016/j.dsr2.2008.07.002.
  20. Glover, A.G., C.R. Smith, S.L. Mincks, P.Y.G. Sumida, and A.R. Thurber. 2008. Macrofaunal abundance and composition on the West Antarctic Peninsula continental shelf: Evidence for a sediment ‘food bank’ and similarities to deep-sea habitats. Deep Sea Research Part II 55:2,491–2,501, https://doi.org/10.1016/j.dsr2.2008.06.008.
  21. Gutt, J., A. Starmans, and G. Dieckmann. 1998. Phytodetritus deposited on the Antarctic shelf and upper slope: Its relevance for the benthic system. Journal of Marine Systems 17:435–444, https://doi.org/10.1016/S0924-7963(98)00054-2.
  22. Hall, S., and S. Thatje. 2010. Temperature-driven biogeography of the deep-sea family Lithodidae (Crustacea: Decapoda: Anomura) in the Southern Ocean. Polar Biology 34:363–370, https://doi.org/10.1007/s00300-010-0890-0.
  23. Hartnett, H., S. Boehme, C. Thomas, D.J. DeMaster, and C. Smith. 2008. Benthic oxygen fluxes and denitrification rates from high-resolution porewater profiles from the Western Antarctic Peninsula continental shelf. Deep Sea Research Part II 55:2,415–2,424, https://doi.org/10.1016/j.dsr2.2008.06.002.
  24. Holm-Hansen, O. 1985. Nutrient cycles in Antarctic marine ecosystems. Pp. 6–10 in Antarctic Nutrient Cycles and Food Webs. W.R. Siegfried, P.R. Condy, and R.M. Laws, eds, Springer-Verlag.
  25. Isla, E., S. Rossi, A. Palanques, J.M. Gili, D. Gerdes, and W. Arntz. 2006. Biochemical composition of marine sediment from the eastern Weddell Sea (Antarctica): High nutritive value in a high benthic-biomass environment. Journal of Marine Systems 60:255–267, https://doi.org/10.1016/j.jmarsys.2006.01.006.
  26. Jacobs, S.S., and J.C. Comiso. 1997. Climate variability in the Amundsen and Bellingshausen Seas. Journal of Climate 10(4):697–709, https://doi.org/10.1175/1520-0442(1997)010<0697:CVITAA>2.0.CO;2.
  27. Karl, D.M., J.R. Christian, J.E. Dore, and R.M. Letelier. 1996. Microbiological oceanography in the region west of the Antarctic Peninsula: Microbial dynamics, nitrogen cycle and carbon flux. Pp. 303–332 in Foundation for Ecological Research West of the Antarctic Peninsula. Antarctic Research Series, vol. 70, R. Ross, E. Hofmann, and L. Quetin, eds, American Geophysical Union, Washington, DC, https://doi.org/10.1029/AR070p0303.
  28. Mayer, L.M., L.L. Schick, T. Sawyer, C.J. Plante, P.A. Jumars, and R.L. Self. 1995. Bioavailable amino acids in sediments: A biomimetic, kinetics-based approach. Limnology and Oceanography 40(3):511–520.
  29. McClintic, M.A., D.J. DeMaster, C.J. Thomas, and C.R. Smith. 2008. Testing the FOODBANCS hypothesis: Seasonal variations in near-bottom particle flux, bioturbation intensity, and deposit feeding based on 234Th measurements. Deep Sea Research Part II 55:2,425–2,437, https://doi.org/10.1016/j.dsr2.2008.06.003.
  30. Meredith, M.P., and J.C. King. 2005. Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophysical Research Letters 32, L19604, https://doi.org/10.1029/2005GL024042.
  31. Mincks, S.L., P.L. Dyal, G.L.J. Paterson, C.R. Smith, and A.G. Glover. 2009. A new species of Aurospio (Polychaeta, Spionidae) from the Antarctic shelf, with analysis of its ecology, reproductive biology and evolutionary history. Marine Ecology 30(2):181–197, https://doi.org/10.1111/j.1439-0485.2008.00265.x.
  32. Mincks, S.L., and C.R. Smith. 2007. Recruitment patterns in Antarctic Peninsula shelf sediments: Evidence of decoupling from seasonal phytodetritus pulses. Polar Biology 30:587–600, https://doi.org/10.1007/s00300-006-0216-4.
  33. Mincks, S.L., C.R. Smith, and D.J. DeMaster. 2005. Persistence of labile organic matter and microbial biomass in Antarctic shelf sediments: Evidence of a sediment food bank. Marine Ecology Progress Series 300:3–19, https://doi.org/10.3354/meps300003.
  34. Mincks, S.L., C.R. Smith, R. Jeffreys, and P.Y. Sumida. 2008. Trophic structure on the West Antarctic Peninsula shelf: Detritivory and benthic inertia revealed by δ13C and δ15N analysis. Deep-Sea Research Part II 55:2,502–2,514, https://doi.org/10.1016/j.dsr2.2008.06.009.
  35. Moline, M.A., H. Claustre, T.K. Frazer, O. Schofield, and M. Vernet. 2004. Alteration of the food web along the Antarctic Peninsula in response to a regional warming trend. Global Change Biology 10:1,973–1,980, https://doi.org/10.1111/j.1365-2486.2004.00825.x.
  36. Montes-Hugo, M., S.C. Doney, H.W. Ducklow, W. Fraser, D. Martinson, S.E. Stammerjohn, and O. Schofield. 2009. Recent changes in phytoplankton communities associated with rapid regional climate change along the Western Antarctic Peninsula. Science 323:1,470–1,473, https://doi.org/10.1126/science.1164533.
  37. Norkko, A., S.F. Thrush, V.J. Cummings, M.M. Gibbs, N.L. Andrew, J. Norkko, and A.M. Schwarz. 2007. Trophic structure of coastal Antarctic food webs associated with changes in sea ice and food supply. Ecology 88(11):2,810–2,820, https://doi.org/10.1890/06-1396.1.
  38. Purinton, B.L., D.J. DeMaster, C.J. Thomas, and C.R. Smith. 2008. 14C as a tracer of labile organic matter in Antarctic benthic food webs. Deep Sea Research Part II 55:2,438–2,450, https://doi.org/10.1016/j.dsr2.2008.06.004.
  39. Robador, A., V. Brüchert, A.D. Steen, and C. Arnosti. 2010. Temperature induced decoupling of enzymatic hydrolysis and carbon remineralization in long-term incubations of Arctic and temperate sediments. Geochimica et Cosmochimica Acta 74(8):2,316–2,326, https://doi.org/10.1016/j.gca.2010.01.022.
  40. Schlesinger, W.H. 1997. Biogeochemistry: An Analysis of Global Change. Academic Press, 588 pp.
  41. Smith, C.R., and D.J. DeMaster, eds. 2008a. FOODBANCS: Food for Benthos along the Antarctic Continental Shelf. Deep Sea Research Part II 55(22–23):2,399–2,534.
  42. Smith, C.R., and D.J. DeMaster. 2008b. Preface and brief synthesis for the FOODBANCS volume. Deep Sea Research Part II 55:2,399–2,403, https://doi.org/10.1016/j.dsr2.2008.08.001.
  43. Smith, C.R., L.J. Grange, D.L. Honig, L. Naudts, B. Huber, L. Guidi, and E. Domack. 2012. A large population of king crabs in Palmer Deep on the west Antarctic Peninsula shelf and potential invasive impacts. Proceedings of the Royal Society B 279:1,017–1,026, https://doi.org/10.1098/rspb.2011.1496.
  44. Smith, C.R., S. Mincks, and D.J. DeMaster. 2006. A synthesis of bentho-pelagic coupling on the Antarctic shelf: Food banks, ecosystem inertia and global climate change. Deep Sea Research Part II 53:875–894, https://doi.org/10.1016/j.dsr2.2006.02.001.
  45. Smith, C.R., S. Mincks, and D.J. DeMaster. 2008. The FOODBANCS project: Introduction and sinking fluxes of organic carbon, chlorophyll-a and phytodetritus on the western Antarctic Peninsula continental shelf. Deep Sea Research Part II 55:2,404–2,414, https://doi.org/10.1016/j.dsr2.2008.06.001.
  46. Smith, C.R., R.H. Pope, D.J. DeMaster, and L. Magaard. 1993. Age-dependent mixing in deep-sea sediments. Geochimica et Cosmochimica Acta 57:1,473–1,488, https://doi.org/10.1016/0016-7037(93)90007-J.
  47. Smith, R.C., K.S. Baker, W.R. Fraser, E.E. Hofmann, and others. 1995. The Palmer LTER: A long-term ecological research program at Palmer Station, Antarctica. Oceanography 8(3):77–86. Available online at: http://tos.org/oceanography/issues/issue_archive/issue_pdfs/8_3/8.3_smith_et_al.pdf (accessed July 2, 2012).
  48. Smith, R.C., H.M. Dierssen, and M. Vernet. 1996. Phytoplankton biomass and productivity in the western Antarctic Peninsula region. Pp. 333–356 in Foundations for Ecological Research West of the Antarctic Peninsula. Antarctic Research Series, vol. 70, E.E. Hofmann, R.M. Ross, and L.B. Quetin, eds, American Geophysical Union, Washington, DC, https://doi.org/10.1029/AR070p0333.
  49. Sumida, P.Y.G., A.F. Bernardino, V.P. Stedall, A.G. Glover, and C.R. Smith. 2008. Temporal changes in benthic megafaunal abundance and composition across the West Antarctic Peninsula shelf: Results from video surveys. Deep Sea Research Part II 55:2,465–2,477, https://doi.org/10.1016/j.dsr2.2008.06.006.
  50. Thatje, S., S. Hall, C. Hauton, C. Held, and P. Tyler. 2008. Encounter of lithodid crab Paralomis birsteini on the continental slope off Antarctica, sampled by ROV. Polar Biology 31(9):1,143–1,148, https://doi.org/10.1007/s00300-008-0457-5.
  51. Thomas, D.N., and G.S. Dieckmann, eds. 2010. Sea Ice, 2nd ed. Wiley-Blackwell, Oxford, UK, 640 pp.
  52. Weston, N.B., and S.B. Joye. 2005. Temperature-driven decoupling of key phases of organic matter degradation in marine sediments. Proceedings of the National Academy of Sciences of the United States of America 102(47):17,036–17,040, https://doi.org/10.1073/pnas.0508798102.
  53. Wheatcroft, R.A., P.A. Jumars, C.R. Smith, and A.R.M. Nowell. 1990. A mechanistic view of the particulate biodiffusion coefficient: Step lengths, rest periods and transport directions. Journal of Marine Research 48(1):177–207, https://doi.org/10.1357/002224090784984560.
  54. Wigham, B.D., E.A. Galley, C.R. Smith, and P.A. Tyler. 2008. Inter-annual variability and potential for selectivity in the diets of deep-water Antarctic echinoderms. Deep Sea Research Part II 55:2,478–2,490, https://doi.org/10.1016/j.dsr2.2008.06.007.
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