Chemoattraction to dimethyl sulfide links the sulfur, iron, and carbon cycles in high-latitude oceans

Abstract

Large marine regions, including the exceptionally productive Southern Ocean, are iron-limited. As a result, there has been substantial interest in iron-fertilizing high nutrient low chlorophyll (HNLC) areas in an effort to sequester atmospheric carbon dioxide. More recently, research has shifted to quantifying the beneficial effects of iron recycling by marine biota. Marine top predators such as whales and seabirds have been examined specifically in this regard as they have high biomass, form dense aggregations, and excrete bioavailable iron in concentrations seven orders of magnitude higher than ambient seawater. Despite it being well established that marine fauna link the iron and carbon cycles, the connection of this process to the sulfur cycle has rarely been considered. The chemoattraction of specific marine fauna to algal-derived dimethyl sulfide (DMS) is key in triggering dense, multi-species foraging aggregations that induce iron recycling, augmenting carbon assimilation. The goal of this paper is twofold; first, to highlight DMS chemoattraction as a behavior that catalyzes carbon sequestration via natural iron fertilization, and second, to identify knowledge gaps that recent biogeochemical advances can address. Fostering this interdisciplinary research will enhance our understanding of global climate regulation, ecosystem services provided by marine top predators, and the biogeochemical cycles of carbon, iron, and sulfur in HNLC waters.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Amin SA, Green DH, Hart MC, Ku FC (2009) Photolysis of iron—siderophore chelates promotes bacterial—algal mutualism. Proc Natl Acad Sci USA 106:17071–17076

    Article  Google Scholar 

  2. Amin SA, Hmelo LR, Van Tol HM, Durham BP, Carlson LT, Heal KR, Morales RL, Berthiaume CT, Parker MS, Djunaedi B, Ingalls AE, Parsek MR, Moran MA, Armbrust EV (2015) Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:98–101. https://doi.org/10.1038/nature14488

    Article  Google Scholar 

  3. Amo L, Rodríguez-Gironés M, Barbosa A (2013) Olfactory detection of dimethyl sulphide in a krill-eating Antarctic penguin. Mar Ecol Prog Ser 474:277–285. https://doi.org/10.3354/meps10081

    Article  Google Scholar 

  4. Anderson ORJ, Phillips RA, Shore RF, McGill RAR, McDonald RA, Bearhop S (2010) Element patterns in albatrosses and petrels: influence of trophic position, foraging range, and prey type. Environ Pollut 158:98–107. https://doi.org/10.1016/j.envpol.2009.07.040

    Article  Google Scholar 

  5. Anderwald P, Evans PGH, Gygax L, Hoelzel AR (2011) Role of feeding strategies in seabird—minke whale associations. Mar Ecol Prog Ser 424:219–227. https://doi.org/10.3354/meps08947

    Article  Google Scholar 

  6. Andreae MO, Raemdonck H (1983) Dimethyl sulfide in the surface ocean and the marine atmosphere: a global view. Science 221:744–747

    Article  Google Scholar 

  7. Asher EC, Merzouk A, Tortell PD (2011) Fine-scale spatial and temporal variability of surface water dimethylsufide (DMS) concentrations and sea-air fluxes in the NE Subarctic Pacific. Mar Chem 126:63–75. https://doi.org/10.1016/j.marchem.2011.03.009

    Article  Google Scholar 

  8. Baker CS, Clapham PJ (2004) Modelling the past and future of whales and whaling. Trends Ecol Evol 19:365–371. https://doi.org/10.1016/j.tree.2004.05.005

    Article  Google Scholar 

  9. Bang B (1966) The olfactory apparatus of tubenosed birds (Procellariiformes). Acta Anat (Basel) 65:391–415

    Article  Google Scholar 

  10. Blain S, Quéguiner B, Armand L, Belviso S, Bombled B, Bopp L, Bowie A, Brunet C, Brussaard C, Carlotti F, Christaki U, Corbière A, Durand I, Ebersbach F, Fuda J-L, Garcia N, Gerringa L, Griffiths B, Guigue C, Guillerm C, Jacquet S, Jeandel C, Laan P, Lefèvre D, Lo Monaco C, Malits A, Mosseri J, Obernosterer I, Park Y-H, Picheral M, Pondaven P, Remenyi T, Sandroni V, Sarthou G, Savoye N, Scouarnec L, Souhaut M, Thuiller D, Timmermans K, Trull T, Uitz J, van Beek P, Veldhuis M, Vincent D, Viollier E, Vong L, Wagener T (2007) Effect of natural iron fertilization on carbon sequestration in the Southern Ocean. Nature 446:1070–1074. https://doi.org/10.1038/nature05700

    Article  Google Scholar 

  11. Bonadonna F, Nevitt GA (2004) Partner-specific odor recognition in an Antarctic seabird. Science 306:835. https://doi.org/10.1126/science.1103001

    Article  Google Scholar 

  12. Bonadonna F, Sanz-Aguilar A (2012) Kin recognition and inbreeding avoidance in wild birds: the first evidence for individual kin-related odour recognition. Anim Behav 84:509–513. https://doi.org/10.1016/j.anbehav.2012.06.014

    Article  Google Scholar 

  13. Bonadonna F, Spaggiari J, Weimerskirch H (2001) Could osmotaxis explain the ability of blue petrels to return to their burrows at night? J Exp Biol 204:1485–1489

    Google Scholar 

  14. Bonadonna F, Caro S, Jouventin P, Nevitt GA (2006) Evidence that blue petrel, Halobaena caerulea, fledglings can detect and orient to dimethyl sulfide. J Exp Biol 209:2165–2169. https://doi.org/10.1242/jeb.02252

    Article  Google Scholar 

  15. Boyd PW, Ellwood MJ (2010) The biogeochemical cycle of iron in the ocean. Nat Geosci 3:675–682. https://doi.org/10.1038/ngeo964

    Article  Google Scholar 

  16. Boyd PW, Watson AJ, Law CS, Abraham ER, Trull T, Murdoch R, Bakker DC, Bowie AR, Buesseler KO, Chang H, Charette M, Croot P, Downing K, Frew R, Gall M, Hadfield M, Hall J, Harvey M, Jameson G, LaRoche J, Liddicoat M, Ling R, Maldonado MT, McKay RM, Nodder S, Pickmere S, Pridmore R, Rintoul S, Safi K, Sutton P, Strzepek R, Tanneberger K, Turner S, Waite A, Zeldis J (2000) A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature 407:695–702. https://doi.org/10.1038/35037500

    Article  Google Scholar 

  17. Boyd PW, Jickells T, Law CS, Blain S, Boyle EA, Buesseler KO, Coale KH, Cullen JJ, de Baar HJW, Follows M, Harvey M, Lancelot C, Levasseur M, Owens NPJ, Pollard R, Rivkin RB, Sarmiento J, Schoemann V, Smetacek V, Takeda S, Tsuda A, Turner S, Watson AJ (2007) Mesoscale iron enrichment experiments 1993-2005: synthesis and future directions. Science 315:612–617. https://doi.org/10.1126/science.1131669

    Article  Google Scholar 

  18. Branch TA, Matsuoka K, Miyashita T (2004) Evidence for increases in antarctic blue whales based on bayesian modelling. Mar Mammal Sci 20:726–754. https://doi.org/10.1111/j.1748-7692.2004.tb01190.x

    Article  Google Scholar 

  19. Breckels MN, Roberts EC, Archer SD, Malin G, Steinke M (2011) The role of dissolved infochemicals in mediating predator-prey interactions in the heterotrophic dinoflagellate Oxyrrhis marina. J Plankton Res 33:629–639. https://doi.org/10.1093/plankt/fbq114

    Article  Google Scholar 

  20. Brooke MDL (2004) The food consumption of the world’s seabirds. Biol Lett 271:S246–S248. https://doi.org/10.1098/rsbl.2003.0153

    Google Scholar 

  21. Charlson RJ, Lovelock JE, Andreae MO, Warren SG (1987) Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326:655–661

    Article  Google Scholar 

  22. Coale KH, Fitzwater SE, Gordon RM, Johnson K, Barber RT (1996) Control of community growth and export production by upwelled iron in the equatorial Pacific Ocean. Nature 379:621–624

    Article  Google Scholar 

  23. Conway TM, John SG (2014) Quantification of dissolved iron sources to the North Atlantic Ocean. Nature 511:212–215. https://doi.org/10.1038/nature13482

    Article  Google Scholar 

  24. Croll D, Marinovic B, Benson S, Chavez F, Black N, Ternullo R, Tershy B (2005) From wind to whales: trophic links in a coastal upwelling system. Mar Ecol Prog Ser 289:117–130. https://doi.org/10.3354/meps289117

    Article  Google Scholar 

  25. 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. Limnol Oceanogr 48:1079–1087. https://doi.org/10.4319/lo.2003.48.3.1079

    Article  Google Scholar 

  26. Cunningham GB, Strauss V, Ryan PG (2008) African penguins (Spheniscus demersus) can detect dimethyl sulphide, a prey-related odour. J Exp Biol 211:3123–3127. https://doi.org/10.1242/jeb.018325

    Article  Google Scholar 

  27. Cunningham GB, Leclaire S, Toscani C, Bonadonna F (2016) Responses of king penguin Aptenodytes patagonicus adults and chicks to two food-related odours. J Avian Biol 47:1–8. https://doi.org/10.1111/jav.00863

    Article  Google Scholar 

  28. Curson ARJ, Todd JD, Sullivan MJ, Johnston AWB (2011) Catabolism of dimethylsulphoniopropionate: Microorganisms, enzymes and genes. Nat Rev Microbiol 9:849–859. https://doi.org/10.1038/nrmicro2653

    Article  Google Scholar 

  29. Cury PM, Boyd IL, Bonhommeau S, Anker-Nilssen T, Crawford RJM, Furness RW, Mills JA, Murphy EJ, Osterblom H, Paleczny M, Piatt JF, Roux J-P, Shannon L, Sydeman WJ (2011) Global seabird response to forage fish depletion–one-third for the birds. Science 334:1703–1706. https://doi.org/10.1126/science.1212928

    Article  Google Scholar 

  30. Dacey JW, Wakeham SG (1986) Oceanic dimethylsulfide: production during zooplankton grazing on phytoplankton. Science 233:1314–1316. https://doi.org/10.1126/science.233.4770.1314

    Article  Google Scholar 

  31. De La Rocha CL (2006) The Biological Pump. In: Holland H, Turekian K (eds) Treatise on Geochemistry. Elsevier Ltd., Oxford, pp 93–122

    Google Scholar 

  32. DeBose JL, Nevitt GA (2008) The use of odors at different spatial scales: comparing birds with fish. J Chem Ecol 34:867–881. https://doi.org/10.1007/s10886-008-9493-4

    Article  Google Scholar 

  33. DeBose JL, Lema SC, Nevitt GA (2008) Dimethylsulfoniopropionate as a foraging cue for reef fishes. Science 319:1356. https://doi.org/10.1126/science.1151109

    Article  Google Scholar 

  34. DeBose JL, Nevitt GA, Dittman AH (2010) Rapid communication: experimental evidence that Juvenile Pelagic Jacks (Carangidae) respond behaviorally to DMSP. J Chem Ecol 36:326–328. https://doi.org/10.1007/s10886-010-9755-9

    Article  Google Scholar 

  35. Dell’Ariccia G, Célérier A, Gabirot M, Palmas P, Massa B, Bonadonna F (2014) Olfactory foraging in temperate waters: sensitivity to dimethylsulphide of shearwaters in the Atlantic Ocean and Mediterranean Sea. J Exp Biol 217:1701–1709. https://doi.org/10.1242/jeb.097931

    Article  Google Scholar 

  36. Dickson DMJ, Kirst GO (1986) The role of β-dimethylsulphoniopropionate, glycine betaine and homarine in the osmoacclimation of Platymonas subcordiformis. Planta 167:536–543. https://doi.org/10.1007/BF00391230

    Article  Google Scholar 

  37. Dove ADM (2015) Foraging and ingestive behaviors of whale sharks, rhincodon typus, in response to chemical stimulus cues. Biol Bull. https://doi.org/10.1086/BBLv228n1p65

    Google Scholar 

  38. Ducklow H, Steinberg D, Buesseler K (2001) Upper ocean carbon export and the biological pump. Oceanography 14:50–58. https://doi.org/10.5670/oceanog.2001.06

    Article  Google Scholar 

  39. Durham BP, Sharma S, Luo H, Smith CB, Amin SA, Bender SJ, Dearth SP, Van Mooy BAS, Campagna SR, Kujawinski EB, Armbrust EV, Moran MA (2015) Cryptic carbon and sulfur cycling between surface ocean plankton. Proc Natl Acad Sci 112:453–457. https://doi.org/10.1073/pnas.1413137112

    Article  Google Scholar 

  40. Ellis JC, Farina JM, Witman JD (2006) Nutrient transfer from sea to land: the case of gulls and cormorants in the gulf of maine. J Anim Ecol 75:565–574

    Article  Google Scholar 

  41. Ellwood MJ, Hutchins DA, Lohan MC, Milne A, Nasemann P, Nodder SD, Sander SG, Strzepek R, Wilhelm SW, Boyd PW (2015) Iron stable isotopes track pelagic iron cycling during a subtropical phytoplankton bloom. Proc Natl Acad Sci USA 112:15–20. https://doi.org/10.1073/pnas.1421576112

    Article  Google Scholar 

  42. Endres CS, Lohmann KJ (2012) Perception of dimethyl sulfide (DMS) by loggerhead sea turtles: a possible mechanism for locating high-productivity oceanic regions for foraging. J Exp Biol 215:3535–3538. https://doi.org/10.1242/jeb.073221

    Article  Google Scholar 

  43. Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, Gruber N, Hibbard K, Högberg P, Linder S, Mackenzie FT, Moore B, Pedersen T, Rosenthal Y, Seitzinger S, Smetacek V, Steffen W (2000) The global carbon cycle: a test of our knowledge of earth as a system. Science 290:291–296. https://doi.org/10.1126/science.290.5490.291

    Article  Google Scholar 

  44. Ferrer RP, Zimmer RK (2012) Community ecology and the evolution of molecules of keystone significance. Biol Bull 223:167–177

    Article  Google Scholar 

  45. Ferrer RP, Zimmer RK (2013) Molecules of keystone significance: crucial agents in ecology and resource management. Bioscience 63:428–438. https://doi.org/10.1525/bio.2013.63.6.5

    Article  Google Scholar 

  46. Foretich MA, Paris CB, Grosell M, Stieglitz JD, Daniel D (2017) Dimethyl sulfide is a chemical attractant for reef fish larvae. Sci Rep. https://doi.org/10.1038/s41598-017-02675-3

    Google Scholar 

  47. Fry B (2006) Stable isotope ecology, 3rd edn. Springer, New York

    Book  Google Scholar 

  48. Gabric A, Murray N, Stone L, Kohl M (1993) Modelling the production of dimethylsulfide during a phytoplankton bloom. J Geophys Res 98:22805–22816. https://doi.org/10.1029/93jc01773

    Article  Google Scholar 

  49. Gilham M (1961) Modification of sub-antarctic flora on Macquarie Island by sea-birds and sea elephants. Proc R Soc Victoria 74:1–12

    Google Scholar 

  50. Godfrey SJ, Geisler J, Fitzgerald EMG (2013) On the olfactory anatomy in an archaic whale (Protocetidae, Cetacea) and the minke whale Balaenoptera acutorostrata (Balaenopteridae, Cetacea). Anat Rec 296:257–272. https://doi.org/10.1002/ar.22637

    Article  Google Scholar 

  51. Gowen RJ, McCullough G, Kleppel GS, Houchin L, Elliott P (1999) Are copepods important grazers of the spring phytoplankton bloom in the western Irish Sea? J Plankton Res 21:465–483. https://doi.org/10.1093/plankt/21.3.465

    Article  Google Scholar 

  52. Gran HH (1931) On the conditions for the production of plankton in the sea. Rapp Procès-Verbaux des Réunions, Cons Int pour l’Exploration la Mer 75:37–46

    Google Scholar 

  53. Grubb TC (1972) Smell and foraging in shearwaters and petrels. Nature 237:404–405

    Article  Google Scholar 

  54. Grubb TC (1973) Colony location by Leach’s Petrel. Auk 90:78–82

    Google Scholar 

  55. Grubb TC (1974) Olfactory navigation to the nesting burrow in Leach’s storm petrel (Oceanodroma leucorhoa). Anim Behav 22:192–202

    Article  Google Scholar 

  56. Hasler HD, Wisby WJ (1951) Discrimination of stream odors by fishes and Its relation to parent stream behavior. Am Nat 85:223–238

    Article  Google Scholar 

  57. Hassler CS, Schoemann V, Nichols CM, Butler ECV, Boyd PW (2011) Saccharides enhance iron bioavailability to Southern Ocean phytoplankton. Proc Natl Acad Sci USA 108:1076–1081. https://doi.org/10.1073/pnas.1010963108

    Article  Google Scholar 

  58. Henson SA, Sanders R, Madsen E, Morris PJ, Le Moigne F, Quartly GD (2011) A reduced estimate of the strength of the ocean’s biological carbon pump. Geophys Res Lett 38:L04606. https://doi.org/10.1029/2011GL046735

    Article  Google Scholar 

  59. Hoffman W, Heinemann D, Wiens JA, Hoffman W, Heinemann D, Wiens JA (1981) The ecology of seabird feeding flocks in alaska. Auk 98:437–456

    Google Scholar 

  60. Humphries GRW, Huettmann F, Nevitt GA, Deal C, Atkinson D (2012) Species distribution modeling of storm-petrels (Oceanodroma furcata and O. leucorhoa) in the North Pacific and the role of dimethyl sulfide. Polar Biol 35:1669–1680. https://doi.org/10.1007/s00300-012-1207-2

    Article  Google Scholar 

  61. Huntley ME, Lopez MD, Karl DM (1991) Top predators in the Southern ocean: a major leak in the biological carbon pump. Science 253:64–66

    Article  Google Scholar 

  62. Hutchins DA (1995) Iron and the marine phytoplankton community. In: Round FE, Chapman DE (eds) Progress in phycological research. Biopress Ltd, New York, pp 1–48

    Google Scholar 

  63. Jickells TD, An ZS, Andersen KK, Baker AR, Bergametti G, Brooks N, Cao JJ, Boyd PW, Duce RA, Hunter KA, Kawahata H, Kubilay N, LaRoche J, Liss PS, Mahowald N, Prospero JM, Ridgwell AJ, Tegen I, Torres R (2005) Global iron connections between desert dust, ocean biogeochemistry, and climate. Science 308:67–71. https://doi.org/10.1126/science.1105959

    Article  Google Scholar 

  64. Joos F, Sarmiento JL, Siegenthaler U (1991) Estimates of the effect of Southern Ocean iron fertilization on atmospheric CO2 concentrations. Nature 349:772–774. https://doi.org/10.1038/349772a0

    Article  Google Scholar 

  65. Jouventin P, Weimerskirch H (1990) Satellite tracking of wandering albatross. Nature 343:746–748

    Article  Google Scholar 

  66. Kirchman D (1996) Microbial ferrous wheel. Nature 383:303–304

    Article  Google Scholar 

  67. Kirst GO, Thiel C, Wolff H, Nothnagel J, Wanzek M, Ulmke R (1991) Dimethylsulfoniopropionate (DMSP) in ice-algae and its possible biological role. Mar Chem 35:381–388. https://doi.org/10.1016/S0304-4203(09)90030-5

    Article  Google Scholar 

  68. Kowalewsky S, Dambach M, Mauck B, Dehnhardt G (2006) High olfactory sensitivity for dimethyl sulphide in harbour seals. Biol Lett 2:106–109. https://doi.org/10.1098/rsbl.2005.0380

    Article  Google Scholar 

  69. Lana A, Bell TG, Simó R, Vallina SM, Ballabrera-Poy J, Kettle AJ, Dachs J, Bopp L, Saltzman ES, Stefels J, Johnson JE, Liss PS (2011) An updated climatology of surface dimethlysulfide concentrations and emission fluxes in the global ocean. Global Biogeochem Cycles 25:1–17. https://doi.org/10.1029/2010GB003850

    Article  Google Scholar 

  70. Lavery TJ, Roudnew B, Gill P, Seymour J, Seuront L, Johnson G, Mitchell JG, Smetacek V (2010) Iron defecation by sperm whales stimulates carbon export in the Southern Ocean. Proc R Soc B 277:3527–3531. https://doi.org/10.1098/rspb.2010.0863

    Article  Google Scholar 

  71. Lavery TJ, Roudnew B, Seymour J, Mitchell JG, Smetacek V, Nicol S (2014) Whales sustain fisheries: blue whales stimulate primary production in the Southern Ocean. Mar Mammal Sci 30:888–904. https://doi.org/10.1111/mms.12108

    Article  Google Scholar 

  72. Lindeboom H (1984) The nitrogen pathway in a penguin rookery. Ecology 65:269–277

    Article  Google Scholar 

  73. Martin JH (1990) Glacial-interglacial CO2 change: the iron hypothesis. Paleoceanography 5:1–13

    Article  Google Scholar 

  74. Martin JH, Fitzwater SE, Gordon RM (1990a) Iron deficiency limits phytoplankton growth in antarctic waters. Global Biogeochem Cycles 4:5–12

    Article  Google Scholar 

  75. Martin JH, Fitzwater SE (1988) Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic. Nature 331:341–343

    Article  Google Scholar 

  76. Martin JH, Gordon RM, Fitzwater SE (1990b) Iron in Antarctic waters. Nature 345:156–158. https://doi.org/10.1016/0021-9797(80)90501-9

    Article  Google Scholar 

  77. Martin P, van der Loeff MR, Cassar N, Vandromme P, D’Ovidio F, Stemmann L, Rengarajan R, Soares M, Gonzalez H, Ebersbach F, Lampitt RS, Sanders R, Barnett B, Smetacek V, Naqvi SWA (2013) Iron fertilization enhanced net community production but not downward particle flux during the Southern Ocean iron fertilization experiment LOHAFEX. Global Biogeochem Cycles. https://doi.org/10.1002/gbc.20077

    Google Scholar 

  78. Mawji E, Schlitzer R, Dodas EM, Abadie C, Abouchami W, Anderson RF, Baars O, Bakker K, Baskaran M, Bates NR, Bluhm K, Bowie A, Bown J, Boye M, Boyle EA, Branellec P, Bruland KW, Brzezinski MA, Bucciarelli E, Buesseler K, Butler E, Cai P, Cardinal D, Casciotti K, Chaves J, Cheng H, Chever F, Church TM, Colman AS, Conway TM, Croot PL, Cutter GA, De Baar HJW, De Souza GF, Dehairs F, Deng F, Dieu HT, Dulaquais G, Echegoyen-Sanz Y, Lawrence Edwards R, Fahrbach E, Fitzsimmons J, Fleisher M, Frank M, Friedrich J, Fripiat F, Galer SJG, Gamo T, Solsona EG, Gerringa LJA, Godoy JM, Gonzalez S, Grossteffan E, Hattaa M, Hayes CT, Heller MI, Henderson G, Huang KF, Jeandel C, Jenkins WJ, John S, Kenna TC, Klunder M, Kretschmer S, Kumamoto Y, Laan P, Labatut M, Lacan F, Lam PJ, Lannuzel D, Le Moigne F, Lechtenfeld OJ, Lohan MC, Lua Y, Masqué P, McClain CR, Measures C, Middag R, Moffett J, Navidad A, Nishioka J, Noble A, Obata H, Ohnemus DC, Owens S, Planchon F, Pradoux C, Puigcorbé V, Quaya P, Radic A, Rehkämper M, Remenyi T, Rijkenberg MJA, Rintoul S, Robinson LF, Roeske T, Rosenberg M, Van Der Loeff MR, Ryabenko E, Saito MA, Roshan S, Salt L, Sarthou G, Schauer U, Scott P, Sedwick PN, Sha L, Shiller AM, Sigman DM, Smethie W, Smith GJ, Sohrin Y, Speich S, Stichel T, Stutsman J, Swift JH, Tagliabue A, Thomas A, Tsunogai U, Twining BS, Van Aken HM, Van Heuven S, Van Ooijen J, Van Weerlee E, Venchiarutti C, Voelker AHL, Wake B, Warner MJ, Woodward EMS, Wu J, Wyatt N, Yoshikawa H, Zheng XY, Xue Z, Zieringer M, Zimmer LA (2014) The GEOTRACES intermediate data product 2014. Mar Chem 177:1–8. https://doi.org/10.1016/j.marchem.2015.04.005

    Article  Google Scholar 

  79. McCauley DJ, DeSalles PA, Young HS, Dunbar RB, Dirzo R, Mills MM, Micheli F (2012) From wing to wing: the persistence of long ecological interaction chains in less-disturbed ecosystems. Sci Rep. https://doi.org/10.1038/srep00409

    Google Scholar 

  80. McCauley DJ, Pinsky ML, Palumbi SR, Estes JA, Joyce FH, Warner RR (2015) Marine defaunation: animal loss in the global ocean. Science 347:1255641. https://doi.org/10.1126/science.1255641

    Article  Google Scholar 

  81. McCoy DT, Burrows SM, Wood R, Grosvenor DP, Elliott SM, Ma P-L, Rasch PJ, Hartmann DL (2015) Natural aerosols explain seasonal and spatial patterns of Southern Ocean cloud albedo. Sci Adv 1:e1500157. https://doi.org/10.1126/sciadv.1500157

    Article  Google Scholar 

  82. Meskhidze N, Nenes A, Chameides WL, Luo C, Mahowald N (2007) Atlantic Southern Ocean productivity: Fertilization from above or below? Global Biogeochem Cycles 21:n/a-n/a. https://doi.org/10.1029/2006gb002711

  83. Mete A, Dorrestein GM, Marx JJ, Lemmens AG, Beynen AC (2001) A comparative study of iron retention in mynahs, doves and rats. Avian Pathol 30:479–486. https://doi.org/10.1080/03079450120078671

    Article  Google Scholar 

  84. Michelutti N, Blais JM, Mallory ML, Brash J, Thienpont J, Kimpe LE, Douglas MSV, Smol JP (2010) Trophic position influences the efficacy of seabirds as metal biovectors. Proc Natl Acad Sci USA 107:10543–10548. https://doi.org/10.1073/pnas.1001333107

    Article  Google Scholar 

  85. Miller TR, Hnilicka K, Dziedzic A, Desplats P, Belas R (2004) Chemotaxis of Silicibacter sp. Strain TM1040 toward dinoflagellate products. Appl Environ Microbiol 70:4692–4701. https://doi.org/10.1128/AEM.70.8.4692

    Article  Google Scholar 

  86. Mongin M, Molina E, Trull TW (2008) Seasonality and scale of the Kerguelen plateau phytoplankton bloom: a remote sensing and modeling analysis of the influence of natural iron fertilization in the Southern Ocean. Deep Sea Res Part II Top Stud Oceanogr 55:880–892. https://doi.org/10.1016/j.dsr2.2007.12.039

    Article  Google Scholar 

  87. Monnahan CC, Branch TA, Punt AE (2015) Do ship strikes threaten the recovery of endangered eastern North Pacific blue whales? Mar Mammal Sci 31:279–297. https://doi.org/10.1111/mms.12157

    Article  Google Scholar 

  88. Moreno AR, Haffa ALM (2014) The impact of fish and the commercial marine harvest on the ocean iron cycle. PLoS ONE 9:10–14. https://doi.org/10.1371/journal.pone.0107690

    Google Scholar 

  89. Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283. https://doi.org/10.1038/nature01610

    Article  Google Scholar 

  90. Nevitt GA (2000) Olfactory foraging by Antarctic procellariiform seabirds: life at high Reynolds numbers. Biol Bull 198:245–253

    Article  Google Scholar 

  91. Nevitt GA (2008) Sensory ecology on the high seas: the odor world of the procellariiform seabirds. J Exp Biol 211:1706–1713. https://doi.org/10.1242/jeb.015412

    Article  Google Scholar 

  92. Nevitt GA (2011) The neuroecology of dimethyl sulfide: a global-climate regulator turned marine infochemical. Integr Comp Bol 51:819–825. https://doi.org/10.1093/icb/icr093

    Article  Google Scholar 

  93. Nevitt GA, Bonadonna F (2005) Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds. Biol Lett 1:303–305. https://doi.org/10.1098/rsbl.2005.0350

    Article  Google Scholar 

  94. Nevitt GA, Haberman K (2003) Behavioral attraction of Leach’s storm-petrels (Oceanodroma leucorhoa) to dimethyl sulfide. J Exp Biol 206:1497–1501. https://doi.org/10.1242/jeb.00287

    Article  Google Scholar 

  95. Nevitt GA, Hunt GL (1996) Olfactory sensitivities of foraging procellariid seabirds in the Aleutian Islands. Chem Senses 21:649–650

    Google Scholar 

  96. Nevitt GA, Veit RR, Kareiva P (1995) Dimethyl sulphide as a foraging cue for Antarctic Procellariiform seabirds. Nature 376:680–682

    Article  Google Scholar 

  97. Nevitt GA, Reid K, Trathan P (2004) Testing olfactory foraging strategies in an Antarctic seabird assemblage. J Exp Biol 207:3537–3544. https://doi.org/10.1242/jeb.01198

    Article  Google Scholar 

  98. Nevitt GA, Losekoot M, Weimerskirch H (2008) Evidence for olfactory search in wandering albatross, Diomedea exulans. Proc Natl Acad Sci USA 105:4576–4581. https://doi.org/10.1073/pnas.0709047105

    Article  Google Scholar 

  99. Nguyen BC, Belviso S, Mihalopoulos N, Gostan J, Nival P (1988) Dimethyl sulfide production during natural phytoplanktonic blooms. Mar Chem 24:133–141. https://doi.org/10.1016/0304-4203(88)90044-8

    Article  Google Scholar 

  100. Nicol S, Bowie A, Jarman S, Lannuzel D, Meiners KM, Van Der Merwe P (2010) Southern Ocean iron fertilization by baleen whales and Antarctic krill. Fish Fish 11:203–209. https://doi.org/10.1111/j.1467-2979.2010.00356.x

    Article  Google Scholar 

  101. Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75

    Article  Google Scholar 

  102. Paine RT (1969) A note on trophic complexity and community stability. Am Nat 103:91–93

    Article  Google Scholar 

  103. Paleczny M, Hammill E, Karpouzi V, Pauly D (2015) Population trend of the world’s monitored seabirds, 1950-2010. PLoS ONE 10:e0129342. https://doi.org/10.1371/journal.pone.0129342

    Article  Google Scholar 

  104. Penn D, Potts WK (1998) Chemical signals and parasite-mediated sexual selection. Trends Ecol Evol 13:391–396. https://doi.org/10.1016/S0169-5347(98)01473-6

    Article  Google Scholar 

  105. 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. https://doi.org/10.1371/journal.pone.0012444

    Article  Google Scholar 

  106. Petrou K, Trimborn S, Rost B, Ralph PJ, Hassler CS (2014) The impact of iron limitation on the physiology of the Antarctic diatom Chaetoceros simplex. Mar Biol 161:925–937. https://doi.org/10.1007/s00227-014-2392-z

    Article  Google Scholar 

  107. Pohnert G, Steinke M, Tollrian R (2007) Chemical cues, defence metabolites and the shaping of pelagic interspecific interactions. Trends Ecol Evol 22:198–204. https://doi.org/10.1016/j.tree.2007.01.005

    Article  Google Scholar 

  108. Pollard RT, Salter I, Sanders RJ, Lucas MI, Moore CM, Mills RA, Statham PJ, Allen JT, Baker AR, Bakker DCE, Charette MA, Fielding S, Fones GR, French M, Hickman AE, Holland RJ, Hughes JA, Jickells TD, Lampitt RS, Morris PJ, Nédélec FH, Nielsdóttir M, Planquette H, Popova EE, Poulton AJ, Read JF, Seeyave S, Smith T, Stinchcombe M, Taylor S, Thomalla S, Venables HJ, Williamson R, Zubkov MV (2009) Southern Ocean deep-water carbon export enhanced by natural iron fertilization. Nature 457:577–580. https://doi.org/10.1038/nature07716

    Article  Google Scholar 

  109. Quinn PK, Bates TS (2011) The case against climate regulation via oceanic phytoplankton sulphur emissions. Nature 480:51–56. https://doi.org/10.1038/nature10580

    Article  Google Scholar 

  110. Raina J-B, Tapiolas DM, Forêt S, Lutz A, Abrego D, Ceh J, Seneca FO, Clode PL, Bourne DG, Willis BL, Motti CA (2013) DMSP biosynthesis by an animal and its role in coral thermal stress response. Nature 502:677–680. https://doi.org/10.1038/nature12677

    Article  Google Scholar 

  111. Ralls K (1971) Mammalian scent marking. Science 171:443–449

    Article  Google Scholar 

  112. Ratnarajah L, Bowie AR, Lannuzel D, Meiners KM, Nicol S (2014) The biogeochemical role of baleen whales and krill in southern ocean nutrient cycling. PLoS ONE 9:e114067. https://doi.org/10.1371/journal.pone.0114067

    Article  Google Scholar 

  113. Ratnarajah L, Melbourne-Thomas J, Marzloff MP, Lannuzel D, Meiners KM, Chever F, Nicol S, Bowie AR (2016a) A preliminary model of iron fertilisation by baleen whales and Antarctic krill in the Southern Ocean: sensitivity of primary productivity estimates to parameter uncertainty. Ecol Modell 320:203–212. https://doi.org/10.1016/j.ecolmodel.2015.10.007

    Article  Google Scholar 

  114. Ratnarajah L, Nicol S, Kawaguchi S, Townsend AT, Lannuzel D, Meiners KM, Bowie AR (2016b) Understanding the variability in the iron concentration of Antarctic krill. Limnol Oceanogr 61:1651–1660. https://doi.org/10.1002/lno.10322

    Article  Google Scholar 

  115. Roman J, McCarthy JJ (2010) The whale pump: marine mammals enhance primary productivity in a coastal basin. PLoS ONE 5:e13255. https://doi.org/10.1371/journal.pone.0013255

    Article  Google Scholar 

  116. Roman J, Palumbi SR (2003) Whales Before Whaling in the North Atlantic. Science 301:60–510. https://doi.org/10.1126/science.1084524

    Article  Google Scholar 

  117. Roman J, Estes JA, Morissette L, Smith C, Costa D, McCarthy J, Nation J, Nicol S, Pershing A, Smetacek V (2014) Whales as marine ecosystem engineers. Front Ecol Environ 12:377–385. https://doi.org/10.1890/130220

    Article  Google Scholar 

  118. Roman J, Nevins J, Altabet M, Koopman H, McCarthy J (2016) Endangered right whales enhance primary productivity in the bay of fundy. PLoS ONE 11:1–14. https://doi.org/10.1371/journal.pone.0156553

    Google Scholar 

  119. Saito H, Tsuda A, Kasai H (2002) Nutrient and plankton dynamics in the Oyashio region of the western subarctic Pacific Ocean. Deep Res Part II Top Stud Oceanogr 49:5463–5486. https://doi.org/10.1016/S0967-0645(02)00204-7

    Article  Google Scholar 

  120. Savoca MS, Nevitt GA (2014) Evidence that dimethyl sulfide facilitates a tritrophic mutualism between marine primary producers and top predators. Proc Natl Acad Sci USA 111:4157–4161. https://doi.org/10.1073/pnas.1317120111

    Article  Google Scholar 

  121. Savoca MS, Wohlfeil ME, Ebeler SE, Nevitt GA (2016) Marine plastic debris emits a keystone infochemical for olfactory foraging seabirds. Sci Adv 2:e1600395. https://doi.org/10.1126/sciadv.1600395

    Article  Google Scholar 

  122. Savoca MS, Tyson CW, Mcgill M, Slager CJ (2017) Odours from marine plastic debris induce food search behaviours in a forage fish. Proc R Soc B 284:20171000. https://doi.org/10.1098/rspb.2017.1000

    Article  Google Scholar 

  123. Schlitzer R (2002) Carbon export fluxes in the Southern Ocean: results from inverse modeling and comparison with satellite-based estimates. Deep Res Part II Top Stud Oceanogr 49:1623–1644. https://doi.org/10.1016/S0967-0645(02)00004-8

    Article  Google Scholar 

  124. Schmidt K, Schlosser C, Atkinson A, Fielding S, Venables HJ, Waluda CM, Achterberg EP (2016) Zooplankton gut passage mobilizes lithogenic iron for ocean productivity. Curr Biol 26:1–7. https://doi.org/10.1016/j.cub.2016.07.058

    Article  Google Scholar 

  125. Seco Pon JP, Beltrame O, Marcovecchio J, Favero M, Gandini P (2012) Assessment of trace metal concentrations in feathers of White-chinned Petrels, Procellaria aequinoctialis, from the Patagonian shelf. Environ Pollut 1:29–37. https://doi.org/10.5539/ep.v1n1p29

    Google Scholar 

  126. Seymour JR, Simó R, Ahmed T, Stocker R (2010) Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 329:342–345. https://doi.org/10.1126/science.1188418

    Article  Google Scholar 

  127. Shaffer SA, Tremblay Y, Weimerskirch H, Scott D, Thompson DR, Sagar PM, Moller H, Taylor GA, Foley DG, Block BA, Costa DP (2006) Migratory shearwaters integrate oceanic resources across the Pacific Ocean in an endless summer. Proc Natl Acad Sci USA 103:12799–12802. https://doi.org/10.1073/pnas.0603715103

    Article  Google Scholar 

  128. Shatova O, Wing SR, Gault-Ringold M, Wing L, Hoffmann LJ (2016) Seabird guano enhances phytoplankton production in the Southern Ocean. J Exp Mar Bio Ecol 483:74–87. https://doi.org/10.1016/j.jembe.2016.07.004

    Article  Google Scholar 

  129. Sieburth JM (1960) Acrylic acid, an “antibiotic” principle in phaeocystis blooms in Antarctic waters. Science 132:676–677

    Article  Google Scholar 

  130. Siegel V (2005) Distribution and population dynamics of Euphausia superba: summary of recent findings. Polar Biol 29:1–22. https://doi.org/10.1007/s00300-005-0058-5

    Article  Google Scholar 

  131. Sigman D (2006) The biological pump in the past. In: Holland H, Turekian K (eds) Treatise on geochemistry. Elsevier Ltd., Oxford, pp 491–528

    Google Scholar 

  132. Simó R (2004) From cells to globe: approaching the dynamics of DMS(P) in the ocean at multiple scales. Can J Fish Aquat Sci 61:673–684. https://doi.org/10.1139/f04-030

    Article  Google Scholar 

  133. Smetacek VS (1985) Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance. Mar Biol 84:239–251. https://doi.org/10.1007/BF00392493

    Article  Google Scholar 

  134. Smetacek V (2008) Are declining Antarctic krill stocks a result of global warming or of the decimation of the whales? In: Duarte CM (ed) Impacts of global warming on polar ecosystems. Fundacion BBVA, Madrid, pp 46–80

    Google Scholar 

  135. Smetacek V, Naqvi SWA (2010) The expedition of the research vessel “Polarstern” to the Antarctic in 2009 (ANT-XXV/3 - LOHAFEX)

  136. Smetacek V, Nicol S (2005) Polar ocean ecosystems in a changing world. Nature 437:362–368. https://doi.org/10.1038/nature04161

    Article  Google Scholar 

  137. Smetacek V, Klaas C, Strass VH, Assmy P, Montresor M, Cisewski B, Savoye N, Webb A, D’Ovidio F, Arrieta JM, Bathmann U, Bellerby R, Berg GM, Croot P, Gonzalez S, Henjes J, Herndl GJ, Hoffmann LJ, Leach H, Losch M, Mills MM, Neill C, Peeken I, Röttgers R, Sachs O, Sauter E, Schmidt MM, Schwarz J, Terbrüggen A, Wolf-Gladrow D (2012) Deep carbon export from a Southern Ocean iron-fertilized diatom bloom. Nature 487:313–319. https://doi.org/10.1038/nature11229

    Article  Google Scholar 

  138. Smith LV, McMinn A, Martin A, Nicol S, Bowie AR, Lannuzel D, van der Merwe P (2013) Preliminary investigation into the stimulation of phytoplankton photophysiology and growth by whale faeces. J Exp Mar Bio Ecol 446:1–9. https://doi.org/10.1016/j.jembe.2013.04.010

    Article  Google Scholar 

  139. Stefels J, Steinke M, Turner S, Malin G, Belviso S (2007) Environmental constraints on the production and removal of the climatically active gas dimethylsulphide (DMS) and implications for ecosystem modelling. Biogeochemistry 83:245–275. https://doi.org/10.1007/s10533-007-9091-5

    Article  Google Scholar 

  140. Steinke M, Malin G, Liss PS (2002) Trophic interactions in the sea: an ecological role for climate relevant volatiles? J Phycol 638:630–638

    Article  Google Scholar 

  141. Steinke M, Stefels J, Stamhuis E (2006) Dimethyl sulfide triggers search behavior in copepods. Limnol Oceanogr 51:1925–1930

    Article  Google Scholar 

  142. Stoeppler M, Brandt K (1979) Comparative studies on trace metal levels in marine biota II. Trace metals in krill, krill products, and fish from the antarctic Scotia Sea. Z Lebensm Unters Forsch 169:95–98

    Article  Google Scholar 

  143. Strzepek RF, Maldonado MT, Higgins JL, Hall J, Safi K, Wilhelm SW, Boyd PW (2005) Spinning the “ferrous wheel”: the importance of the microbial community in an iron budget during the FeCycle experiment. Global Biogeochem Cycles. https://doi.org/10.1029/2005GB002490

    Google Scholar 

  144. Szefer P, Szefer K, Pempkowiak J, Skwarzec B, Bojanowski R, Holm E (1994) Distribution and coassociations of selected metals in seals of the Antarctic. Environ Pollut 83:341–349. https://doi.org/10.1016/0269-7491(94)90156-2

    Article  Google Scholar 

  145. Tagliabue A, Bowie AR, Boyd PW, Buck KN, Johnson KS, Saito MA (2017) The integral role of iron in ocean biogeochemistry. Nature 543:51–59. https://doi.org/10.1038/nature21058

    Article  Google Scholar 

  146. Thewissen JGM, George J, Rosa C, Kishida T (2011) Olfaction and brain size in the bowhead whale (Balaena mysticetus). Mar Mammal Sci 27:282–294. https://doi.org/10.1111/j.1748-7692.2010.00406.x

    Article  Google Scholar 

  147. Tovar-Sanchez A, Duarte CM, Hernández-León S, Sañudo-Wilhelmy SA (2007) Krill as a central node for iron cycling in the Southern Ocean. Geophys Res Lett 32:L11601. https://doi.org/10.1029/2006GL029096

    Article  Google Scholar 

  148. Vos M, Vet LEM, Wäckers FL, Middelburg JJ, van der Putten WH, Mooij WM, Heip CHR, van Donk E (2006) Infochemicals structure marine, terrestrial and freshwater food webs: implications for ecological informatics. Ecol Inform 1:23–32. https://doi.org/10.1016/j.ecoinf.2005.06.001

    Article  Google Scholar 

  149. Vroom RJE, Koelmans AA, Besseling E, Halsband C (2017) Aging of microplastics promotes their ingestion by marine zooplankton. Environ Pollut 231:987–996. https://doi.org/10.1016/j.envpol.2017.08.088

    Article  Google Scholar 

  150. Warham J (1990) The petrels: their ecology and breeding systems. Academic Press, New York

    Google Scholar 

  151. Wing S, Jack L, Shatova O, Leichter J, Barr D, Frew R, Gault-Ringold M (2014) Seabirds and marine mammals redistribute bioavailable iron in the Southern Ocean. Mar Ecol Prog Ser 510:1–13. https://doi.org/10.3354/meps10923

    Article  Google Scholar 

  152. Wing S, Wing L, Shatova O, Van Hale R (2017a) Marine micronutrient vectors: seabirds, marine mammals and fishes egest high concentrations of bioactive metals in the subantarctic island ecosystem. Mar Ecol Prog Ser 563:13–23. https://doi.org/10.3354/meps11978

    Article  Google Scholar 

  153. Wing SR, Gault-Ringold M, Stirling CH, Wing LC, Shatova OA, Frew RD (2017b) δ 56 Fe in seabird guano reveals extensive recycling of iron in the Southern Ocean ecosystem. Limnol Oceanogr 62:1671–1681. https://doi.org/10.1002/lno.10524

    Article  Google Scholar 

  154. Wolfe GV, Steinke M (1996) Grazing-activated production of dimethyl sulfide (DMS) by two clones of Emiliania huxleyi. Limnol Oceanogr 41:1151–1160. https://doi.org/10.4319/lo.1996.41.6.1151

    Article  Google Scholar 

  155. Wolfe GV, Strom SL, Holmes JL, Radzio T, Olson MB (2002) Dimethylsulphoniopropionate cleavage by marine phytoplankton in response to mechanical, chemical, or dark stress. J Phycol 38:948–960

    Article  Google Scholar 

  156. Worm B, Hilborn R, Baum JK, Branch TA, Collie JS, Costello C, Fogarty MJ, Fulton EA, Hutchings JA, Jennings S, Jensen OP, Lotze HK, Mace PM, McClanahan TR, Minto C, Palumbi SR, Parma AM, Ricard D, Rosenberg AA, Watson R, Zeller D (2009) Rebuilding global fisheries. Science 325:578–585. https://doi.org/10.1126/science.1173146

    Article  Google Scholar 

  157. Wright KLB, Pichegru L, Ryan PG (2011) Penguins are attracted to dimethyl sulphide at sea. J Exp Biol 214:2509–2511. https://doi.org/10.1242/jeb.058230

    Article  Google Scholar 

Download references

Acknowledgements

I am grateful to Gabrielle Nevitt for initial discussions on the manuscript and to Sarah Maclean and Allison Bruce for generating illustrations used in Figs. 1 and 3. I would also like to thank Grant Humphries for assistance in creating Fig. 2 and Rachel Anderson for editorial assistance. Finally, I would like to thank the three anonymous reviewers whose feedback improved the manuscript considerably.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Matthew S. Savoca.

Additional information

Responsible Editor: Marc G .Kramer.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Savoca, M.S. Chemoattraction to dimethyl sulfide links the sulfur, iron, and carbon cycles in high-latitude oceans. Biogeochemistry 138, 1–21 (2018). https://doi.org/10.1007/s10533-018-0433-2

Download citation

Keywords

  • Marine biogeochemistry
  • Community ecology
  • Polar biology
  • Iron cycle
  • Carbon cycle
  • Dimethyl sulfide
  • Top predators