The trophic and metabolic pathways of foraminifera in the Arabian Sea: Evidence from cellular stable isotopes

Biogeosciences

Volumn 12, Issue 6, 2015, Pages 1781-1797

  Jeffreys, R M ^a   Fisher, E H ^a   Gooday, A J ^b   Larkin, K E ^c   Billett, D S M ^d   Wolff, G A ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c Marine Board Wandelaarkaai 7 ^*  (Belgium)

^d Deep Seas Environmental Solutions Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM; BENTHIC FAUNA; BENTHOS; CHEMOSYNTHESIS; DETRITUS; FOOD AVAILABILITY; FORAMINIFERA; ISOTOPIC COMPOSITION; JELLYFISH; METABOLISM; OXYGEN MINIMUM LAYER; PARTICULATE ORGANIC MATTER; PRODUCTIVITY; SEAFLOOR; STABLE ISOTOPE;

ARABIAN SEA; INDIAN OCEAN; OMAN; PAKISTAN;

CRAMBIONELLA ORSINI; FORAMINIFERA; SCYPHOZOA;

EID: 84925047579     PISSN: 17264170     EISSN: 17264189     Source Type: Journal    
DOI: 10.5194/bg-12-1781-2015     Document Type: Article

References (97)

1. 14N ratios, Nature, 373, 506-509, 1995.
2. Aranada da Silva, A. and Gooday, A. J.: Large organic-walled Protista (Gromia) in the Arabian Sea Density, diversity, distribution and ecology, Deep-Sea Res. Pt. II, 56, 422-433, 2009.
3. Bernhard, J. M., Edgcomb, V. P., Casciotti, K. L., McIlvin, M. R., and Beaudoin, D. J.: Denitrification likely catalyzed by endobionts in an allogromiid foraminifer, ISME J., 6, 951-960, 2011.
4. Bernhard, J. M., Casciotti, K. L., McIlvin, M. R., Beaudoin, D. J., Visscher, P. T., and Edgcomb, V. P.: Potential importance of physiologically diverse benthic foraminifera in sedimentary nitrate storage and respiration, J. Geophys. Res., 117, G03002, doi:10.1029/2012JG001949, 2012.
5. Billett, D., Lampitt, R., Rice, A., and Mantoura, R.: Seasonal Sedimentation of Phytoplankton to the Deep-Sea Benthos, Nature, 302, 520-522, 1983.
6. Billett, D. S. M., Bett, B. J., Jacobs, C. L., Rouse, I. P., andWigham, B. D.: Mass deposition of jellyfish in the deep Arabian Sea, Limnol. Oceanogr., 51, 2077-2083, 2006.
7. Brand, T. D. and Griffiths, C.: Seasonality in the hydrography and biogeochemistry across the Pakistan margin of the NE Arabian Sea, Deep-Sea Res. Pt. II, 56, 283-295, 2009.
8. Brandes, J., Devol, A., Yoshinari, T., Jayakumar, D., and Naqvi, S.: Isotopic composition of nitrate in the central Arabian Sea and eastern tropical North Pacific: A tracer for mixing and nitrogen cycles, Limnol. Oceanogr., 43, 1680-1689, 1998.
9. Breuer, E. R., Law, G. T. W., Woulds, C., Cowie, G. L., Shimmield, G. B., Peppe, O., Schwartz, M., and Mckinlay, S.: Sedimentary oxygen consumption and microdistribution at sites across the Arabian Sea oxygen minimum zone (Pakistan margin), Deep-Sea Res. Pt. II, 56, 296-304, 2009.
10. Brooks, J. M., Kennicutt, M. C., Fisher, C. R., Macko, S. A., Cole, K., Childress, J. J., Bidigare, R. R., and Vetter, R. D.: Deep-Sea Hydrocarbon Seep Communities: Evidence for Energy and Nutritional Carbon Sources, Science, 238, 1138-1142, 1987.
11. Burkill, P. H., Mantoura, R., and Owens, N.: Biogeochemical cycling in the northwestern Indian Ocean: A brief overview, Deep-Sea Res. Pt. II, 40, 643-649, 1993.
12. Campbell, B., Stein, J., and Cary, S.: Evidence of chemolithoautotrophy in the bacterial community associated with Alvinella pompejana, a hydrothermal vent polychaete, Appl. Environ. Microb., 69, 5070-5078, 2003.
13. Cline, J. D. and Kaplan, I. R.: Isotopic fractionation of dissolved nitrate during denitrification in the eastern tropical north pacific ocean, Mar. Chem., 3, 271-299, 1975.
14. Cook, A., John D Lambshead, P., Hawkins, L., Mitchell, N., and Levin, L.: Nematode abundance at the oxygen minimum zone in the Arabian Sea, Deep-Sea Res. Pt. II, 47, 75-85, 2000.
15. Cowie, G.: The biogeochemistry of Arabian Sea surficial sediments: A review of recent studies, Prog. Oceanogr., 65, 260-289, 2005.
16. Cowie, G., Calvert, S., Pedersen, T., Schulz, H., and Rad, von, U.: Organic content and preservational controls in surficial shelf and slope sediments from the Arabian Sea (Pakistan margin), Mar. Geol., 161, 23-38, 1999.
17. Cowie, G. L. and Levin, L. A.: Benthic biological and biogeochemical patterns and processes across an oxygen minimum zone (Pakistan margin, NE Arabian Sea), Deep-Sea Res. Pt. II, 56, 261-270, 2009.
18. Cowie, G. L., Mowbray, S., Lewis, M., Matheson, H., and Mckenzie, R.: Carbon and nitrogen elemental and stable isotopic compositions of surficial sediments from the Pakistan margin of the Arabian Sea, Deep-Sea Res. Pt. II, 56, 271-282, 2009.
19. Dannheim, J., Struck, U. and Brey, T.: Does sample bulk freezing affect stable isotope ratios of infaunal macrozoobenthos?, J. Exp. Mar. Bio. Ecol., 351, 37-41, 2007.
20. Decker, C. and Olu, K.: Habitat heterogeneity influences cold-seep macrofaunal communities within and among seeps along the Norwegian margin - Part 2: contribution of chemosynthesis and nutritional patterns, Mar. Ecol., 33, 231-245, 2011.
21. Demopoulos, A. W. J., Gualtieri, D., and Kovacs, K.: Food-web structure of seep sediment macrobenthos from the Gulf of Mexico, Deep-Sea Res. Pt. II, 57, 1972-1981, 2010.
22. DeNiro, M. J. and Epstein, S.: Influence of diet on the distribution of carbon isotopes in animals, Geochim. Cosmochim. Ac., 42, 495-506, 1978.
23. DeNiro, M. and Epstein, S.: Influence of Diet on the Distribution of Nitrogen Isotopes in Animals, Geochim. Cosmochim. Ac., 45, 341-351, 1981.
24. Enge, A., Nomaki, H., Ogawa, N., Witte, U., Moeseneder, M., Lavik, G., Ohkouchi, N., Kitazato, H., Kǔcera, M., and Heinz, P.: Response of the benthic foraminiferal community to a simulated short-term phytodetritus pulse in the abyssal North Pacific, Mar. Ecol.-Prog. Ser., 438, 129-142, 2011.
25. Feuchtmayr, H. and Grey, J.: Effect of preparation and preservation procedures on carbon and nitrogen stable isotope determinations from zooplankton, Rapid Commun Mass Spectrom., 17, 2605-2610, 2003.
26. Findlater, J.: A major low-level air current near the Indian Ocean during the northern summer, Q. J. Roy. Meteor. Soc., 95, 362-380, 1969.
27. 13C measurements as indicators of carbon flow in marine and freshwater ecosystems, Contrib. Mar. Sci., 27, 13-47, 1984.
28. Gaye-Haake, B., Lahajnar, N., Emeis, K., Unger, D., Rixen, T., Suthhof, A., Ramaswamy, V., Schulz, H., Paropkari, A., and Guptha, M.: Stable nitrogen isotopic ratios of sinking particles and sediments from the northern Indian Ocean, Mar. Chem., 96, 243-255, 2005.
29. Gillan, F. T. and Johns, R. B.: Chemical markers for marine bacteria: fatty acids and pigments, Meth. Geoch., 24, 291-309, 1986.
30. Glock, N., Schönfeld, J., Eisenhauer, A., Hensen, C., Mallon, J., and Sommer, S.: The role of benthic foraminifera in the benthic nitrogen cycle of the Peruvian oxygen minimum zone, Biogeosciences, 10, 4767-4783, doi:10.5194/bg-10-4767-2013, 2013.
31. Goes, J., Thoppil, P., Gomes, H., and Fasullo, J.: Warming of the Eurasian landmass is making the Arabian Sea more productive, Science, 308, 545-547, 2005.
32. Gooday, A.: A Response by Benthic Foraminifera to the Deposition of Phytodetritus in the Deep-Sea, Nature, 332, 70-73, 1988.
33. Gooday, A.: Biological responses to seasonally varying fluxes of organic matter to the ocean floor: a review, J. Oceanogr., 58, 305-332, 2002.
34. Gooday, A. J., Levin, L. A., Linke, P., and Heeger, T.: The role of benthic foraminifera in deep-sea food webs and carbon cycling, in: Deep-sea food chains and the global carbon cycle, Springer Netherlands, Dordrecht, 63-91, 1992.
35. Gooday, A. J., Bernhard, J. M., Levin, L. A., and Suhr, S. B.: Foraminifera in the Arabian Sea oxygen minimum zone and other oxygen-deficient settings: taxonomic composition, diversity, and relation to metazoan faunas, Deep-Sea Res. Pt. II, 47, 25-54, 2000.
36. Gooday, A. J., Pond, D. W., and Bowser, S. S.: Ecology and nutrition of the large agglutinated foraminiferan Bathysiphon capillare in the bathyal NE Atlantic: distribution within the sediment profile and lipid biomarker composition, Mar. Ecol.-Prog. Ser., 245, 69-82, 2002.
37. Gooday, A. J., Nomaki, H., and Kitazato, H.: Modern deep-sea benthic foraminifera: a brief review of their morphology-based biodiversity and trophic diversity, Geol. Soc. Spec. Publ., 303, 97-119, 2008.
38. Gooday, A. J., Levin, L. A., Silva, A. A. D., Bett, B. J., Cowie, G. L., Dissard, D., Gage, J. D., Hughes, D. J., Jeffreys, R., Lamont, P. A., Larkin, K. E., Murty, S. J., Schumacher, S., Whitcraft, C., and Woulds, C.: Faunal responses to oxygen gradients on the Pakistan margin A comparison of foraminiferans, macrofauna and megafauna, Deep-Sea Res. Pt. II, 56, 488-502, 2009.
39. Graf, G.: Benthic Pelagic Coupling in a Deep-Sea Benthic Community, Nature, 341, 437-439, 1989.
40. Grandel, S., Rickert, D., Schlüter, M., and Wallmann, K.: Porewater distribution and quantification of diffusive benthic fluxes of silicic acid, nitrate and phosphate in surface sediments of the deep Arabian Sea, Deep-Sea Res. Pt. II, 47, 2707-2734, 2000.
41. Gupta, R. S. and Naqvi, S.: Chemical oceanography of the Indian Ocean, north of the equator, Deep-Sea Res. Pt. I, 31, 671-706, 1984.
42. Haake, B., Ittekkot, V., Rixen, T., Ramaswamy, V., Nair, R., and Curry, W.: Seasonality and Interannual Variability of Particle Fluxes to the Deep Arabian Sea, Deep-Sea Res. Pt. I, 40, 1323-1344, 1993.
43. Hansen, H. P.: Determination of oxygen, in: Methods in Seawater Analysis, Wiley-VCH Verlag, Weinheim, Germany, 75-89, 1999.
44. Hedges, J. I. and Keil, R. G.: Sedimentary organic matter preservation: an assessment and speculative synthesis, Mar. Chem., 49, 81-115, 1995.
45. 15N analysis, Mar. Ecol.-Prog. Ser., 84, 9-18, 1992.
46. Honjo, S., Dymond, J., Prell, W., and Ittekkot, V.: Monsoon controlled export fluxes to the interior of the Arabian Sea, Deep-Sea Res. Pt. II, 46, 1859-1902, 1999.
47. Honjo, S., Manganini, S. J., and Krishfield, R. A.: Particulate organic carbon fluxes to the ocean interior and factors controlling the biological pump: A synthesis of global sediment trap programs since 1983, Prog. Oceanogr., 76, 217-285, 2008.
48. Iken, K., Brey, T., Wand, U., Voigt, J., and Junghans, P.: Food web structure of the benthic community at the Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis, Prog. Oceanogr., 50, 383-405, 2001.
49. Jørgensen, B. B. and Gallardo, V. A.: Thioploca spp.: filamentous sulfur bacteria with nitrate vacuoles, FEMS Microbiol. Ecol., 28, 301-313, 1999.
50. Jeffreys, R. M.,Wolff, G. A., and Cowie, G. L.: Influence of oxygen on heterotrophic reworking of sedimentary lipids at the Pakistan margin, Deep-Sea Res. Pt. II, 56, 358-375, 2009a.
51. Jeffreys, R. M., Wolff, G. A., and Murty, S. J.: The trophic ecology of key megafaunal species at the Pakistan Margin: Evidence from stable isotopes and lipid biomarkers, Deep-Sea Res. Pt. I, 56, 1816-1833, 2009b.
52. Jeffreys, R. M., Levin, L. A., Lamont, P. A., Woulds, C., Whitcraft, C. R., Mendoza, G. F.,Wolff, G. A., and Cowie, G. L.: Living on the edge: single-species dominance at the Pakistan oxygen minimum zone boundary, Mar. Ecol.-Prog. Ser., 470, 79-99, 2012.
53. Kamykowski, D. and Zentara, S.-J.: Hypoxia in the world ocean as recorded in the historical data set, Deep-Sea Res. Pt. I, 37, 1861-1874, 1990.
54. Koho, K. A., Pina-Ochoa, E., Geslin, E., and Risgaard-Petersen, N.: Vertical migration, nitrate uptake and denitrification: survival mechanisms of foraminifers (Globobulimina turgida) under low oxygen conditions, FEMS Microbiol. Ecol., 75, 273-283, 2010.
55. Larkin, K. E.: Community and trophic responses of benthic foraminifera to oxygen gradients and organic enrichment, PhD thesis, University of Southampton, 323 pp., 2006.
56. Larkin, K. E. and Gooday, A. J., Foraminiferal faunal responses to monsoon-dirven changes in organic matter and oxygen availability at 140 and 300m water depth in the NE Arabian Sea, Deep-Sea Res. Pt. II, 56, 403-421, 2009.
57. Larkin, K. E., Gooday, A. J.,Woulds, C., Jeffreys, R. M., Schwartz, M., Cowie, G., Whitcraft, C., Levin, L., Dick, J. R., and Pond, D. W.: Uptake of algal carbon and the likely synthesis of an "essential" fatty acid by Uvigerina ex. gr. semiornata (Foraminifera) within the Pakistan margin oxygen minimum zone: evidence from fatty acid biomarker and 13C tracer experiments, Biogeosciences, 11, 3729-3738, doi:10.5194/bg-11-3729-2014, 2014.
58. Levin, L. and Michener, R.: Isotopic evidence for chemosynthesisbased nutrition of macrobenthos: The lightness of being at Pacific methane seeps, Limnol. Oceanogr., 1336-1345, 2002.
59. Levin, L., Gage, J., Lamont, P., Cammidge, L., Martin, C., Patience, A. and Crooks, J.: Infaunal community structure in a low-oxygen, organic-rich habitat on the Oman continental slope, NW Arabian Sea, in: The responses of marine organisms to their environments: Proceedings of the 30th European Marine Biology Symposium, University of Southampton, Southampton, UK, 223-230, 1997.
60. Levin, L. A.: Oxygen minimum zone benthos: adaptation and community response to hypoxia, Oceanogr. Mar. Biol., 41, 1-45, 2003.
61. Lipps, J. H. and Valentine, J. W.: The role of foraminifera in the trophic structure of marine communities, Lethaia, 3, 279-286, 1970.
62. Macko, S. A. and Estep, M. L.: Microbial alteration of stable nitrogen and carbon isotopic compositions of organic matter, Org. Geochem., 6, 787-790, 1984.
63. Macko, S. A., Fogel, M. L., Hare, P. E., and Hoering, T. C.: Isotopic fractionation of nitrogen and carbon in the synthesis of amino acids by microorganisms, Chem. Geol., 65, 79-92, 1987.
64. McCutchan, J., Lewis, W., Kendall, C., and McGrath, C.: Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur, Oikos, 102, 378-390, 2003.
65. McGoldrick, D. J., Barton, D. R., Power, M., Scott, R.W., and Butler, B. J.: Dynamics of bacteria-substrate stable isotope separation: dependence on substrate availability and implications for aquatic food web studies, Can. J. Fish. Aquat. Sci., 65, 1983-1990, 2008.
66. 15N and animal age, Geochim. Cosmochim. Ac., 48, 1135-1140, 1984.
67. Mojtahid, M., Zubkov, M. V., Hartmann, M., and Gooday, A. J.: Grazing of intertidal benthic foraminifera on bacteria: assessment using pulse-chase radiotracing, J. Exp. Mar. Biol. Ecol., 399, 25-34, 2011.
68. Moodley, L., Middelburg, J. J., and Boschker, H.: Bacteria and Foraminifera: key players in a short-term deep-sea benthic response to phytodetritus, Mar. Ecol.-Prog. Ser., 236, 23-29, 2002.
69. Murray, J. W.: Ecology and Applications of Benthic Foraminifera, Cambridge Univ Press, Cambridge, UK, 440 pp., 2006.
70. Nair, R., Ittekkot, V., Manganini, S., Ramaswamy, V., Haake, B., Degens, E., Desai, B., and Honjo, S.: Increased particle flux to the deep ocean related to monsoons, Nature, 338, 749-751, 1989.
71. Nomaki, H., Heinz, P., Hemleben, C., and Kitazato, H.: Behaviour and response of deep-sea benthic foraminifera to freshly supplied organic matter: A laboratory feeding experiment in microcosm environments, J. Foram. Res., 35, 103-113, 2005.
72. 13C-labeled bacteria and algae by deep-sea benthic foraminifera, Mar. Ecol.-Prog. Ser., 310, 95-108, 2006.
73. Nomaki, H., Ogawa, N., Ohkouchi, N., Suga, H., Toyofuku, T., Shimanaga, M., Nakatsuka, T., and Kitazato, H.: Benthic foraminifera as trophic links between phytodetritus and benthic metazoans: carbon and nitrogen isotopic evidence, Mar. Ecol.-Prog. Ser., 357, 153-164, 2008.
74. Peters, K. E.: Guidelines for evaluating petroleum source rock using programmed pyrolysis, Am. Assoc. Petr. Geol. B., 70, 318-329, 1986.
75. Pina-Ochoa, E., Hogslund, S., Geslin, E., Cedhagen, T., Revsbech, N. P., Nielsen, L. P., Schweizer, M., Jorissen, F., Rysgaard, S., and Risgaard-Petersen, N.: Widespread occurrence of nitrate storage and denitrification among Foraminifera and Gromiida, P. Natl. Acad. Sci. USA, 107, 1148-1153, 2010.
76. Post, D.: Using stable isotopes to estimate trophic position: Models, methods, and assumptions, Ecology, 83, 703-718, 2002.
77. Prokopenko, M. G., Sigman, D. M., Berelson, W. M., Hammond, D. E., Barnett, B., Chong, L., and Townsend-Small, A.: Denitrification in anoxic sediments supported by biological nitrate transport, Geochim. Cosmochim. Ac., 75, 7180-7199, 2011.
78. Prokopenko, M. G., Hirst, M. B., De Brabandere, L., Lawrence, D. J. P., Berelson, W. M., Granger, J., Chang, B. X., Dawson, S., Crane, E. J., III, Chong, L., Thamdrup, B., Townsend-Small, A., and Sigman, D. M.: Nitrogen losses in anoxic marine sediments driven by Thioploca - anammox bacterial consortia, Nature, 500, 194-198, 2013.
79. 2 fixation in the North Atlantic Ocean?, Global Biogeochem. Cy., 21, GB4015, doi:10.1029/2006GB002886, 2007.
80. Risgaard-Petersen, N., Langezaal, A. M., Ingvardsen, S., Schmid, M. C., Jetten, M. S. M., Op den Camp, H. J., Derksen, J. W. M., Pina-Ochoa, E., Eriksson, S. P., Nielsen, L. P., Revsbech, N. P., Cedhagen, T., and van der Zwaan, J.: Evidence for complete denitrification in a benthic foraminifera, Nature, 443, 93-96, 2006.
81. Robinson, J. J. and Cavanaugh, C. M.: Expression of form I and form II Rubisco in chemoautotrophic symbioses: implications for the interpretation of stable carbon isotope values, Limnol. Oceanogr., 40, 1496-1502, 1995.
82. Ryther, J. H., Hall, J. R., Pease, A. K., Bakun, A., and Jones, M. M.: Primary organic production in relation to the chemistry and hydrography of the western Indian Ocean, Limnol. Oceanogr., 371-380, 1966.
83. Sackett,W., Eckleman,W. R., Bender, M., and Be, A. H.: Temperature dependence of carbon isotope composition in marine plankton and sediments, Science, 148, 235-237, 1965.
84. Schmaljohann, R., Drews, M., Walter, S., Linke, P., Rad, von, U., and Imhoff, J.: Oxygen-minimum zone sediments in the northeastern Arabian Sea off Pakistan: a habitat for the bacterium Thioploca, Mar. Ecol.-Prog. Ser., 211, 27-42, 2001.
85. Schott, F. A. and McCreary, J. P., Jr: The monsoon circulation of the Indian Ocean, Prog. Oceanogr., 51, 1-123, 2001.
86. Smallwood, B. andWolff, G.: Molecular characterisation of organic matter in sediments underlying the oxygen minimum zone at the Oman Margin, Arabian Sea, Deep-Sea Res. Pt. II, 47, 353-375, 2000.
87. Smith, C., Hoover, D., Doan, S., Pope, R., DeMaster, D., Dobbs, F., and Altabet, M.: Phytodetritus at the abyssal seafloor across 10 degrees of latitude in the central equatorial Pacific, Deep-Sea Res. Pt. II, 43, 1309-1338, 1996.
88. Smith, S. L. and Codispoti, L. A.: Southwest monsoon of 1979: Chemical and biological response of Somali coastal waters, Science, 209, 597-600, 1980.
89. Suhr, S. B., Pond, D. W., Gooday, A. J., and Smith, C. R.: Selective feeding by benthic foraminifera on phytodetritus on the western Antarctic Peninsula shelf: evidence from fatty acid biomarker analysis, Mar. Ecol.-Prog. Ser., 262, 153-162, 2003.
90. Tendal, O. S.: Aspects of the biology of Komokiacea and Xenophyophoria, Sarsia, 64, 13-17, 1979.
91. Tyler, P. A.: Seasonality in the deep sea, Oceanogr. Mar. Biol. Ann. Rev., 26, 227-258, 1988.
92. van der Weijden, C. H., Reichart, G. J., and Visser, H. J.: Enhanced preservation of organic matter in sediments deposited within the oxygen minimum zone in the northeastern Arabian Sea, Deep-Sea Res. Pt. I, 46, 807-830, 1999.
93. Velinsky, D. J., Fogel, M. L., Todd, J. F., and Tebo, B. M.: Isotopic fractionation of dissolved ammonium at the oxygen-hydrogen sulfide interface in anoxic waters, Geophys. Res. Lett., 18, 649-652, 1991.
94. Webb, K. L. and Johannes, R. E.: Studies of the release of dissolved free amino acids by marine zooplankton, Limnol. Oceanogr., 376-382, 1967.
95. West, E.,Welsh, D., and Pitt, K.: Influence of decomposing jellyfish on the sediment oxygen demand and nutrient dynamics, Hydrobiologia, 616, 151-160, 2009.
96. Woulds, C., Cowie, G. L., Levin, L. A., Andersson, J. H., Middelburg, J. J., Vandewiele, S., Lamont, P. A., Larkin, K. E., Gooday, A. J., Schumacher, S., Whitcraft, C., Jeffreys, R. M., and Schwartz, M.: Oxygen as a control on seafloor biological communities and their roles in sedimentary carbon cycling, Limnol. Oceanogr., 52, 1698-1709, 2007.
97. Woulds, C., Schwartz, M. C., Brand, T., Cowie, G. L., Law, G., and Mowbray, S. R.: Porewater nutrient concentrations and benthic nutrient fluxes across the Pakistan margin OMZ, Deep-Sea Res. Pt. II, 56, 333-346, 2009.