The biogeochemical role of baleen whales and krill in Southern Ocean nutrient cycling

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Ratnarajah, Lavenia ^a,b   Bowie, Andrew R ^a,b   Lannuzel, Delphine ^a,b   Meiners, Klaus M ^b,c   Nicol, Stephen ^a,b  

^a UNIVERSITY OF TASMANIA   (Australia)

^b UNIVERSITY OF TASMANIA   (Australia)

^c AUSTRALIAN ANTARCTIC DIVISION   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CADMIUM; CARBON; CHLOROPHYLL; COBALT; COPPER; IRON; MANGANESE; PHOSPHORUS; TRACE METAL; ZINC; METAL; SEA WATER; TRACE ELEMENT;

ANIMAL TISSUE; ARTICLE; BIOGEOCHEMICAL CYCLING; CONCENTRATION (PARAMETERS); DEFECATION; FECES ANALYSIS; HIGH NUTRIENT LOW CHLOROPHYLL; KRILL; MASS SPECTROMETRY; NONHUMAN; NUTRIENT CYCLING; NUTRIENT SUPPLY; WHALE; ANIMAL; CHEMISTRY; ECOSYSTEM; FECES; METABOLISM; MUSCLE; PROCEDURES;

EUPHAUSIACEA; MYSTICETI;

ANIMALS; CARBON; ECOSYSTEM; EUPHAUSIACEA; FECES; MASS SPECTROMETRY; METALS; MICRONUTRIENTS; MUSCLES; PHOSPHORUS; SEAWATER; TRACE ELEMENTS; WHALES;

EID: 84915746778     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114067     Document Type: Article

References (70)

1. Moore JK, Abbott MR (2000) Phytoplankton chlorophyll distributions and primary production in the Southern Ocean. Journal of Geophysical Research: Oceans, 105: 28709-28722
2. Frederiksen M, Edwards M, Richardson AJ, Halliday NC, Wanless S (2006) From plankton to top predators: bottom-up control of a marine food web across four trophic levels. Journal of Animal Ecology, 75: 1259-1268
3. Perissinotto R (1997) In situ grazing rates and daily ration of Antarctic krill Euphausia superba feeding on phytoplankton at the Antarctic Polar Front and the Marginal Ice Zone. Marine ecology. Progress series (Halstenbek), 160: 77
4. Sheldon RW, Sutcliffe Jr WH, Paranjape MA (1977) Structure of Pelagic Food Chain and Relationship Between Plankton and Fish Production. Journal of the Fisheries Research Board of Canada, 34: 2344-2353
5. Blain S, Queguiner B, Armand L, Belviso S, Bombled B, et al. (2007) Effect of natural iron fertilization on carbon sequestration in the Southern Ocean. Nature, 446: 1070-4
6. Boyd PW, Watson AJ, Law CS, Abraham ER, Trull T, et al. (2000) A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature, 407: 695-702
7. Morel FMM, Rueter JG, Price NM (1991) Iron nutrition of phytoplankton and its possible importance in the ecology of ocean regions with high nutrient and low biomass. Oceanography (Washington, D.C.), 4: 56
8. SCOR Working Group (2007) GEOTRACES - an international study of the global marine biogeochemical cycles of trace elements and their isotopes. Chemie der Erde - Geochemistry, 67: 85-131
9. Morel FMM, Milligan AJ, Saito MA (2003) Marine bioinorganic chemistry: the role of trace metals in the oceanic cycles of major nutrients. The Oceans and Marine Geochemistry. Treatise on Geochemistry, ed. H Elderfield., Oxford: Elsevier.
10. Morel FMM, Price NM (2003) The biogeochemical cycles of trace metals in the oceans. Science 300: 944-7
11. Landing WM, Bruland KW (1987) The contrasting biogeochemistry of iron and manganese in the Pacific Ocean. Geochimica et Cosmochimica Acta, 51: 29-43
12. Orians KJ, Bruland KW (1986) The biogeochemistry of aluminum in the Pacific Ocean. Earth and Planetary Science Letters, 78: 397-410
13. Coale KH, Johnson KS, Fitzwater SE (1996) A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial pacific ocean. Nature, 383: 495-501
14. Chester R (1990) Trace elements in the oceans, in Marine Geochemistry. Springer Netherlands. p. 346-421.
15. Huntley ME, Lopez MDG, Karl DM (1991) Top Predators in the Southern Ocean: A Major Leak in the Biological Carbon Pump. Science, 253: 64-66
16. Nicol S, Bowie A, Jarman SN, Lannuzel D, Meiners KM, et al. (2010) Southern Ocean iron fertilization by baleen whales and Antarctic krill. Fish and Fisheries, 11: 203-209
17. Jennings S, Wilson RW (2009) Fishing impacts on the marine inorganic carbon cycle. Journal of Applied Ecology, 46: 976-982
18. Lavery TJ, Roudnew B, Gill P, Seymour J, Seuront L, et al. (2010) Iron defecation by sperm whales stimulates carbon export in the Southern Ocean. Proceedings of the Royal Society. B, Biological sciences, 277: 3527-31
19. Pershing AJ, Christensen LB, Record NR, Sherwood GD, Stetson PB (2010) The impact of whaling on the ocean carbon cycle: why bigger was better. PLoS One, 5: e12444
20. Wing SR, Jack L, Shatova O, Leichter JJ, Barr D, et al. (2014) Seabirds and marine mammals redistribute bioavailable iron in the Southern Ocean. Marine Ecology Progress Series, 510: 1-13
21. Spicer JI, Saborowski R (2010) Physiology and Metabolism of Northern Krill (Meganyctiphanes norvegica Sars). Advances in Marine Biology, ed. M Lesser. Vol. 57.: Elsevier.
22. Ordway GA, Garry DJ (2004) Myoglobin: an essential hemoprotein in striated muscle. The Journal of Experimental Biology, 207: 3441-3446
23. Kooyman GL, Castellini MA, Davis RW (1981) Physiology of diving in marine mammals. Annual Review of Physiology, 43: 343-356
24. Roman J, McCarthy JJ (2010) The Whale Pump: Marine Mammals Enhance Primary Productivity in a Coastal Basin. PloS one, 5: e13255
25. Clarke A, Tyler PA (2008) Adult Antarctic Krill Feeding at Abyssal Depths. Current Biology, 18: 282-285
26. Smetacek V, Nicol S (2005) Polar ocean ecosystems in a changing world. Nature, 437: 362-8
27. Smith LV, McMinn A, Martin A, Nicol S, Bowie AR, et al. (2013) Preliminary investigation into the stimulation of phytoplankton photophysiology and growth by whale faeces. Journal of Experimental Marine Biology and Ecology, 446: 1-9
28. Katija K (2012) Biogenic inputs to ocean mixing. The Journal of Experimental Biology, 215: 1040-1049
29. Jarman SN, Gales NJ, Tierney M, Gill PC, Elliott NG (2002) A DNA-based method for identification of krill species and its application to analysing the diet of marine vertebrate predators Molecular ecology, 11: 2679-2690
30. Cullen JT, Sherrell RM (1999) Techniques for determination of trace metals in small samples of size fractionated particulate matter: phytoplankton metals of central California Marine Chemistry, 67: 233-247
31. Townsend AT (2000) The accurate determination of the first row transition metals in water, urine, plant, tissue and rock samples by sector field ICP-MS. Journal of Analytical Spectometry, 15: 307-314
32. Cullen JT, Chase Z, Coale KH, Fitzwater SE, Sherrell RM (2003) Effect of iron limitation on the cadmium to phosphorus ratio of natural phytoplankton assemblages from the Southern Ocean. Limnology Oceanography, 48: 1079-1087
33. Redfield AC (1958) THE BIOLOGICAL CONTROL OF CHEMICAL FACTORS IN THE ENVIRONMENT. American Scientist, 46: 230A-221
34. Barbante C, Cozzi G, Capodaglio G, Cescon P (2000) Trace element determination in a candidate reference material (Antarctic Krill) by ICP-sector field MS. Journal of Analytical Atomic Spectrometry, 15: 377-382
35. Yamamoto Y, Honda K, Tatsukawa R (1987) Heavy metal accumulation in Antarctic krill, Euphausia superba. Polar Biology, 1: 198-204
36. Szefer P, Szefer K, Pempkowiak J, Skwarzec B, Bojanowski R, et al. (1994) Distribution and coassociations of selected metals in seals of the Antarctic. Environmental Pollution, 83: 341-349
37. Honda K, Yamamoto Y, Tatsukawa R (1987) Distribution of heavy metals in Antarctic marine ecosystems. Polar Biol, 1: 184-197
38. Espejo W, Celis JE, Gonzalez-Acuna D, Jara S, Barra R (2014) Concentration of trace metals in excrements of two species of penguins from different locations of the Antarctic Peninsula. Polar biology, 37: 675-683
39. Sandmann G (1985) Consequences of iron deficiency on photosynthetic and respiratory electron transport in blue-green algae. Photosynthesis Research, 6: 261-271
40. Sunda WG, Huntsman SA (1997) Interrelated influence of iron, light and cell size on marine phytoplankton growth. Nature, 390: 389-392
41. Boyd PW, Jickells T, Law CS, Blain S, Boyle EA, et al. (2007) Mesoscale Iron Enrichment Experiments 1993-2005: Synthesis and Future Directions. Science, 315: 612-617
42. de Baar HJW, Boyd PW, Coale KH, Landry MR, Tsuda A, et al. (2005) Synthesis of iron fertilization experiments: From the Iron Age in the Age of Enlightenment. Journal of Geophysical Research: Oceans, 110: C09S16
43. de Baar HJW, de Jong JTM, Bakker DCE, Loscher BM, Veth C, et al. (1995) Importance of iron for plankton blooms and carbon dioxide drawdown in the Southern Ocean. Nature, 373: 412-415
44. Bowie AR, Maldonado MT, Frew R, Croot PL, Achterberg EP, et al. (2001) The fate of added iron during a mesoscale fertilisation experiment in the Southern Ocean. Deep Sea Research II, 48: 2703-2743
45. Corami F, Capodaglio G, Turetta C, Soggia F, Magi E, et al. (2005) Summer distribution of trace metals in the western sector of the Ross Sea, Antarctica. Journal of Environmental Monitoring, 7: 1256-1264
46. Planquette H, Sherrell RM, Stammerjohn S, Field MP (2013) Particulate iron delivery to the water column of the Amundsen Sea, Antarctica. Marine Chemistry, 153: 15-30
47. Twining BS, Baines SB (2004) Element stoichiometries of individual plankton cells collected during the Southern Ocean Iron Experiment(SOFeX). Limnology and oceanography, 49: 2115
48. Baden SP, Eriksson SP (2006) Role, Routes and Effects of Manganese in Crustaceans. Oceanography and Marine Biology, 44: 61-83
49. Fadely BS, Worthy GAJ, Costa DP (1990) Assimilation Efficiency of Northern Fur Seals Determined Using Dietary Manganese. The Journal of Wildlife Management, 54: 246-251
50. Reinfelder JR (2010) Carbon Concentrating Mechanisms in Eukaryotic Marine Phytoplankton. Annual Review of Marine Science, 3: 291-315
51. Lane TW, Morel FMM (2000) A biological function for cadmium in marine diatoms. Proceedings of the National Academy of Sciences, 97: 4627-4631
52. Nemoto T, Okiyama M, Iwasaki N, Kikuchi T (1988) Squid as Predators on Krill (Euphausia superba) and Prey for Sperm Whales in the Southern Ocean, in Antarctic Ocean and Resources Variability, D Sahrhage, Editor, Springer Berlin Heidelberg. p. 292-296.
53. Annett AL, Lapi S, Ruth TJ, Maldonado MT (2008) The Effects of Cu and Fe Availability on the Growth and Cu:C Ratios of Marine Diatoms. Limnology and Oceanography, 53: 2451-2461
54. Sunda WG, Guillard RRL (1976) The relationship between cupric ion activity and the toxicity of copper to phytoplankton. Journal of Marine Research, 37: 761-777
55. Anderson DM, Morel FMM (1978) Copper sensitivity of Gonyaulax-tamarensis. Limnology and Oceanography, 23: 283-295
56. Van Mooy BAS, Fredricks HF, Pedler BE, Dyhrman ST, Karl DM, et al. (2009) Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature, 458: 69-72
57. Nicol S, Stolp M (1991) Molting, Feeding, and Fluoride Concentration of the Antarctic Krill Euphausia superba Dana. Journal of Crustacean Biology, 11: 10-16
58. Lavery TJ, Roudnew B, Seymour J, Mitchell JG, Smetacek V, et al. (2014) Whales sustain fisheries: Blue whales stimulate primary production in the Southern Ocean. Marine Mammal Science, 30: 888-904
59. Smetacek V (2008) Are declining Antarctic krill stocks a result of global warming or of the decimation of the whales. Impacts of global warming on polar ecosystems.: Fundaciön BBVA.
60. Branch TA, Matsuoka K, Miyashita T (2004) Evidence for increases in Antarctic blue whales based on Bayesian modelling. Marine Mammal Science, 20: 726-754
61. International Whaling Commission (2000) Report of the Sub-Committee on the Comprehensive Assessment of Other Whale Stocks - Annex G. Journal of Cetacean Research and Management 2 (Suppl.): 167-208
62. Roman J, Estes JA, Morissette L, Smith C, Costa D, et al. (2014) Whales as marine ecosystem engineers. Frontiers in Ecology and the Environment:
63. Hendry KR, Meredith MP, Measures CI, Carson DS, Rickaby REM (2010) The role of sea ice formation in cycling of aluminium in northern Marguerite Bay, Antarctica. Estuarine, Coastal and Shelf Science, 87: 103-112
64. Fitzwater SE, Johnson KS, Gordon RM, Coale KH, Smith Jr WO (2000) Trace metal concentrations in the Ross Sea and their relationship with nutrients and phytoplankton growth. Deep-sea research. Part II, Topical studies in oceanography, 47: 3159-3179
65. Grotti M, Soggia F, Abelmoschi ML, Rivaro P, Magi E, et al. (2001) Temporal distribution of trace metals in Antarctic coastal waters. Marine Chemistry, 76: 189-209
66. Westerlund S, Öhman P (1991) Iron in the water column of the Weddell Sea. Marine Chemistry, 35: 199-217
67. Löscher BM, de Jong JTM, de Baar HJW (1998) The distribution and preferential biological uptake of cadmium at 6°W in the Southern Ocean. Marine Chemistry, 62: 259-286
68. Löscher BM (1999) Relationships among Ni, Cu, Zn, and major nutrients in the Southern Ocean. Marine Chemistry, 67: 67-102
69. Frew R, Bowie A, Croot P, Pickmere S (2001) Macronutrient and trace-metal geochemistry of an in situ iron-induced Southern Ocean bloom. Deep-sea research. Part II, Topical studies in oceanography, 48: 2467-2481
70. Lannuzel D, Bowie AR, van der Merwe PC, Townsend AT, Schoemann V (2011) Distribution of dissolved and particulate metals in Antarctic sea ice. Marine Chemistry, 124: 134-146