Marine Biodiversity

, Volume 44, Issue 1, pp 5–25 | Cite as

Agglutinated foraminifera (superfamily Hormosinacea) across the Indian margin oxygen minimum zone (Arabian Sea)

  • Amy TaylorEmail author
  • Andrew J. Gooday
Original Paper


We present a semi-quantitative survey of ‘live’ (stained) and dead hormosinacean foraminifera at six sites (500–2,000 m water depth; bottom-water oxygen concentrations 0.007–2.43 ml L−1) across the Indian margin oxygen minimum zone (OMZ). Abundance of stained and dead specimens was highest at 800 m followed by 1,100 m, lowest at 2,000 m (stained) and 500 m (dead). The peak at 800 m possibly represents a release from oxygen stress combined with a rich food supply (‘edge effect’). We recognised 31 species (27 Reophax, 2 Hormosinella, 1 Hormosina and 1 Nodosinella) among the 605 stained and dead specimens; the majority (21) are apparently undescribed. Species richness was low at 2,000 m; within the OMZ, it was maximal at 1,100 m and minimal at 500 m for both stained and dead populations. Three species (R. agglutinatus, R. aff. bilocularis and R. dentaliniformis) occurred across the entire depth range. However, most species were either confined to the 2,000-m site or to one or more sites within the OMZ. Multivariate analysis of assemblage composition revealed that the 2,000-m site was distinct from shallower sites. Within the OMZ, the 900- and 1,100-m sites were the most similar, and the 500-m site the most distinct. Stained:dead test ratios were maximal at 500–835 m, perhaps reflecting enhanced preservation of cytoplasm at very low oxygen concentrations. At least two Reophax species are common to the Indian and Pakistan margin OMZ; one of these may be confined to the core of the Arabian Sea OMZ.


Reophax Indian Ocean OMZ Hypoxia Continental margin 



We thank the captain and crew of the RV “Yokosuka” and the pilots and staff of the “Shinkai 6500” for their assistance with the field operations. We thank the scientists participating in RV “Yokosuka” cruise YK08-11 for their assistance, especially Kazumasa Oguri and Hisami Suga, who generously provided the environmental data in Table 1, Lisa Levin, Hidetaka Nomaki and Ursula Witte for permission to cite their unpublished observations, and Will Hunter, Lisa Levin, Hidetaka Nomaki, Ursula Witte and Claire Woulds, who helped with the faunal work at sea. We thank Dr Kate Larkin for permission to use her photographs of Pakistan margin Reophax species (Figs. 5, 6). Two anonymous reviewers made helpful comments that improved the manuscript. We are particularly grateful to Hiroshi Kitazato for inviting one of us (A.J.G.) to participate in YK08-11.


  1. Akimoto K, Hattori M, Uematsu K, Kato C (2001) The deepest living foraminifera, Challenger Deep, Mariana Trench. Mar Micropaleontol 42:95–97Google Scholar
  2. Aranda da Silva AAS (2005) Benthic Protozoa community attributes in relation to environmental gradients in the Arabian Sea. PhD thesis, University of SouthamptonGoogle Scholar
  3. Bernhard JM (1988) Post-mortem vital staining in benthic foraminifera; duration and importance in population and distributional studies. J Foramin Res 18:143–146CrossRefGoogle Scholar
  4. Bernhard JM, Sen Gupta BK, Borne P (1997) Benthic foraminifera as a proxy to estimate dysoxic bottom-water concentrations, Santa Barbara Basin, U.S. Pacific continental margin. J Foramin Res 27:301–310CrossRefGoogle Scholar
  5. Bernhard, JM, Sen Gupta BK (1999) Foraminifera of oxygen-depleted environments. In: Sen Gupta BK (ed) Modern foraminifera, Kluwer, Dordrecht, pp. 201–216Google Scholar
  6. Bernhard JM, Habura A, Bowser SS (2006) An endobiont-bearing allogromiid from the Santa Barbara Basin: implications for the early diversification of foraminifera. J Geophys Res 111, G03002. doi: 10.1029/2005JG000158
  7. Boulinier T, Nichols JD, Sauer JR, Hines JE, Pollock KH (1998) Estimating species richness: the importance of heterogeneity in species detectability. Ecology 79:1018–1028CrossRefGoogle Scholar
  8. Brady HB (1879) Notes on the reticularian Rhizopoda of the ‘Challenger’ expedition. I. On new and little known arenaceous types. Q J Microsc Sci 19:20–63Google Scholar
  9. Brady HB (1884) Report on the Foraminifera dredged by H.M.S Challenger during the years 1873–1876. Report of the scientific results of the voyage of H.M.S. Challenger, 1873–1876. Zoology 9:1–814Google Scholar
  10. Brönnimann P, Whittaker JE (1980) A revision of Reophax and its type species with remarks on several other recent hormosinids (Protozoa: Foraminifera) in the collections of the British Museum (Natural History). Bull Br Mus Nat Hist Zool 39:259–272Google Scholar
  11. Burmistrova II (1976) Benthic foraminifera in the deep-sea sediments of the Arabian Sea. Oceanology 16:394–396Google Scholar
  12. Cedhagen T (1993) Taxonomy and biology of Pelosina arborescens with comparative notes on Astrorhiza limicola (Foraminifera). Ophelia 37:143–162CrossRefGoogle Scholar
  13. Cushman J (1912) New arenaceous Foraminifera from the Philippine Islands and contiguous waters. Proc US Nat Hist Mus 42:227–230CrossRefGoogle Scholar
  14. Cushman J (1918) The Foraminifera of the Atlantic Ocean Part 1. Astrorhizidae. Bull US Nat Hist Mus 104:1–39Google Scholar
  15. Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia - review of ecological effects and behavioral responses on macrofauna. Oceanogr Mar Biol Annu Rev 33:245–303Google Scholar
  16. Den Dulk M, Reichart GJ, Van Heyst S, Zachariasse WJ, Van der Zwaan, GJ (2000) Benthic foraminifera as proxies of organic matter flux and bottom water oxygenation? A case history from the northern Arabian Sea. Palaeogeogr Palaeoclimatol Palaeoecol 161:337–359Google Scholar
  17. Erbacher J, Nelskamp S (2006) Comparison of benthic foraminifera inside and outside a sulphur-oxidising bacterial mat from the present oxygen-minimum zone off Pakistan (NE Arabian Sea). Deep-Sea Res I 53:751–775CrossRefGoogle Scholar
  18. Flint JM (1899) Recent foraminifera. A descriptive catalogue of specimens dredged by the U.S. Fish Commission steamer Albatross. Rep US Nat Mus for 1897:249–349Google Scholar
  19. Fontanier C, Metzger E, Waelbroeck C, Joufreau M, LeFloch N, Jorissen F, Etcheber H, Bichon S, Chabaud G, Poirier D, Grémare A, Deflandre B (2013) Live (stained) benthic foraminifera off Walvis Bay, Namibia: a deep-sea ecosystem under the influence of bottom nepheloid layers. J Foramin Res 43:55–71CrossRefGoogle Scholar
  20. Geslin E, Heinz P, Hemleben Ch (2004) Behaviour of Bathysiphon sp. and Siphonammina bertholdii n.gen n.sp. under controlled oxygen conditions in the laboratory: implication for bioturbation. In: Bubik M, Kaminski MA (eds) 2004. Proceedings of the Sixth International Workshop on Agglutinated Foraminifera, Grzybowski Foundation Special Publication 8:105–118Google Scholar
  21. Gooday AJ (2003) Benthic foraminifera (Protista) as tools in deep-water palaeoceanography: environmental influences on faunal characteristics. Adv Mar Biol 46:1–90Google Scholar
  22. Gooday AJ, Hughes JA (2002) Foraminifera associated with phytodetritus deposits at a bathyal site in the northern Rockall Trough (NE Atlantic): seasonal contrasts and comparison of stained and dead assemblages. Mar Micropaleontol 46:83–110CrossRefGoogle Scholar
  23. Gooday AJ, Bernhard JM, Levin LA, Suhr SB (2000) Foraminifera in the Arabian Sea oxygen minimum zone and other oxygen-deficient settings: taxonomic composition, diversity, and relation to metazoan faunas. Deep-Sea Res II 47:25–54CrossRefGoogle Scholar
  24. Gooday AJ, Jorissen F, Levin LA, Middelburg JJ, Naqvi SWA, Rabalais NN, Scranton M, Zhang J (2009a) Historical records of coastal eutrophication-induced hypoxia. Biogeosciences 6:1707–1745CrossRefGoogle Scholar
  25. Gooday AJ, Levin LA, Aranda da Silva A, Bett BJ, Cowie GL, Dissard D, Gage JD, Hughes DJ, Jeffreys R, Lamont PA, Larkin KE, Murty SJ, Schumacher S, Whitcraft C, Woulds C (2009b) Faunal responses to oxygen gradients on the Pakistan margin: a comparison of foraminiferans, macrofauna and megafauna. Deep-Sea Res II 56:488–502CrossRefGoogle Scholar
  26. Gooday AJ, Bett BJ, Escobar E, Ingole B, Levin LA, Neira C, Raman AV, Sellanes J (2010a) Biodiversity and habitat heterogeneity in oxygen minimum zones. Mar Ecol 31:125–147CrossRefGoogle Scholar
  27. Gooday AJ, Malzone MG, Bett BJ, Lamont PA (2010b) Decadal-scale changes in shallow-infaunal foraminiferal assemblages at the Porcupine Abyssal Plain, NE Atlantic. Deep-Sea Res II 57:1362–1382CrossRefGoogle Scholar
  28. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391CrossRefGoogle Scholar
  29. Heinz P, Hemleben C (2003) Regional and seasonal variations of recent benthic deep-sea foraminifera in the Arabian Sea. Deep-Sea Res I 50:435–447CrossRefGoogle Scholar
  30. Heinz P, Hemleben C (2006) Foraminiferal response to the Northeast Monsoon in the western and southern Arabian Sea. Mar Micropaleontol 58:103–113CrossRefGoogle Scholar
  31. Helly JJ, Levin LA (2004) Global distribution of naturally occurring marine hypoxia on continental margins. Deep-Sea Res I 51:1159–1168CrossRefGoogle Scholar
  32. Hermelin JOR, Shimmield GB (1990) The importance of the oxygen minimum zone and sediment geochemistry in the distribution of recent benthic foraminifera in the Northwest Indian Ocean. Mar Geol 91:1–29CrossRefGoogle Scholar
  33. Hess S, Kuhnt W, Hill S, Kaminski MA, Holbourn A, de Leon M (2001) Monitoring the recolonization of the Mt Pinatubo 1991 ash layer by benthic foraminifera. Mar Micropaleontol 43:119–142CrossRefGoogle Scholar
  34. Hofker J (1972) Primitive Agglutinated Foraminifera. Brill, LeidenGoogle Scholar
  35. Hunter WR (2011) Epi-benthic megafaunal zonation across an oxygen minimum zone at the Indian continental margin. Deep-Sea Res I 58:699–710CrossRefGoogle Scholar
  36. Ingole BS, Sautya S, Sivades S, Singh R, Nanajkar M (2010) Macrofaunal community structure in the western Indian continental margin including the oxygen minimum zone. Mar Ecol 31:148–166CrossRefGoogle Scholar
  37. Jannink NT, Zachariasse WJ, Van der Zwan GJ (1998) Living (Rose Bengal stained) benthic foraminifera from the Pakistan continental margin (northern Arabian Sea). Deep-Sea Res I 45:1483–1513CrossRefGoogle Scholar
  38. Jorissen FJ (1999) Benthic foraminiferal microhabitats below the sediment water interface. In: Sen Gupta BK (ed) Modern Foraminifera. Kluwer, Norwell, pp 161–180Google Scholar
  39. Jorissen FJ, Wittling I (1999) Ecological evidence from taphonomical studies; living-dead comparisons of benthic foraminiferal faunas off Cape Blanc (NW Africa). Palaeogeogr Palaeoclimatol Palaeoecol 149:151–170CrossRefGoogle Scholar
  40. Jorissen FJ, de Stigter HC, Widmark JGV (1995) A conceptual model explaining benthic foraminiferal microhabitats. Mar Micropaleontol 19:131–146CrossRefGoogle Scholar
  41. Kaminski MA, Boersma A, Tyszka J, Holbourn AEL (1995) Response of deep-water agglutinated foraminifera to dysoxic conditions in the California borderland basins. In: Proceedings of the 4th International Workshop on Agglutinated Foraminifera. Grzybowski Foundation Spec Publ 3:131–140Google Scholar
  42. Kaminski MA, Grassle JF, Whitlatch RB (1988) Life history and recolonization among agglutinated foraminifera in the Panama Basin. In: Gradstein FM, Rögl F (eds) Proceedings of the 2nd International Workshop on Agglutinated Foraminifera. Abhandlungen der Geologischen Bundesanstalt, Wien, 41:229–244Google Scholar
  43. Kamykowski D, Zentara SJ (1990) Hypoxia in the world ocean as recorded in the historical data set. Deep-Sea Res 37:1861–1874CrossRefGoogle Scholar
  44. Karstensen J, Stramma L, Visbeck M (2008) Oxygen minimum zones in the eastern tropical Atlantic and Pacific oceans. Prog Oceanogr 77:331–350CrossRefGoogle Scholar
  45. Kurbjeweit F, Hemleben CH, Schmiedl G, Schiebel R, Pfannkuche O, Wallmann K, Schafer P (2000) Distribution, biomass and diversity of benthic foraminifera in relation to sediment geochemistry in the Arabian Sea. Deep-Sea Res II 47:2913–2955CrossRefGoogle Scholar
  46. Larkin KE (2006) Community and trophic responses of benthic foraminifera to oxygen gradients and organic enrichment. Dissertation, University of SouthamptonGoogle Scholar
  47. Larkin KE, Gooday AJ (2009) Foraminiferal faunal responses to monsoon driven changes in organic matter and oxygen availability at 140 and 300 m water depth in the NE Arabian Sea. Deep-Sea Res II 56:403–421CrossRefGoogle Scholar
  48. Loeblich AR, TappanH (1987) Foraminiferal genera and their classification. Van Nostra and Reinhold, New YorkGoogle Scholar
  49. Levin LA (2003) Oxygen minimum zone benthos: adaptation and community response to hypoxia. Oceanogr Mar Biol Annu Rev 41:1–45Google Scholar
  50. Levin LA (2005) Deep-Ocean life where oxygen is scarce. Am Sci 90:436–444CrossRefGoogle Scholar
  51. Levin LA, Gage JD (1998) Relationships between oxygen, organic matter and the diversity of bathyal macrofauna. Deep-Sea Res II 45:129–163CrossRefGoogle Scholar
  52. Levin LA, Childers SE, Smith CR (1991) Epibenthic, agglutinating foraminiferans in the Santa Catalina Basin and their response to disturbance. Deep-Sea Res 38:465–483CrossRefGoogle Scholar
  53. Levin LA, Gage J, Lamont P, Cammidge L, Martin C, Patience A, Crooks J (1997) Infaunal community structure in a low-oxygen, organic rich habitat on the Oman continental slope, NW Arabian Sea. In: Hawkins L, Hutchinson S (eds) Responses of marine organisms to their environments: proceedings of the 30th European Marine Biology Symposium. University of Southampton, United Kingdom, pp 223–230Google Scholar
  54. Levin LA, Rathburn AE, Neira C, Sellanes J, Munoz P, Gallardo V, Salamanca M (2002) Benthic processes on the Peru margin: a transect across the oxygen-minimum zone during the 1997–1998 El Niño. Prog Oceanogr 53:1–27CrossRefGoogle Scholar
  55. Meadows A, Meadows PS, West FJC, Murray JMH (2000) Bioturbation, geochemistry and geotechnics of sediments affected by the oxygen minimum zone on the Oman continental slope and abyssal plain, Arabian Sea. Deep-Sea Res II 47:259–280CrossRefGoogle Scholar
  56. Milliman JD, Troy PJ, Balch WM, Adams AK, Li YH, Mackenzie FT (1999) Biologically mediated dissolution of calcium carbonate above the chemical lysocline? Deep-Sea Res I 46:1653–1669CrossRefGoogle Scholar
  57. Murray JW (1991) Ecology and palaeoecology of benthic foraminifera. Wiley, New YorkGoogle Scholar
  58. Murray JW, Bowser SE (2000) Mortality, protoplasm decay rate, and reliability of staining techniques to recognise “living” foraminifera: a review. J Foramin Res 30:66–70CrossRefGoogle Scholar
  59. Nozawa F, Kitazato H, Tsuchiya M, Gooday AJ (2006) ‘Live’ benthic foraminifera at an abyssal site in the equatorial Pacific nodule province: abundance, diversity and taxonomic composition. Deep-Sea Res I 53:1406–1422Google Scholar
  60. Oliver PG (2001) Functional morphology and description of a new species of Amygdalum (Mytiloidea) from the oxygen-minimum zone of the Arabian Sea. J Molluscan Stud 67:225–241CrossRefGoogle Scholar
  61. Phleger FB, Soutar A (1973) Production of benthic foraminifera in three east Pacific oxygen minima. Micropaleontology 19:110–115Google Scholar
  62. Reichart GL, Lourens LJ, Zachariasse WJ (1998) Temporal variability in the northern Arabian Sea oxygen-minimum zone during the last 225,000 years. Paleoceanography 13:607–621CrossRefGoogle Scholar
  63. Resig JM, Glenn CR (1997) Foraminifera encrusting phosphoritic hardgrounds of the Peruvian upwelling zone: taxonomy, geochemistry, and distribution. J Foramin Res 27:133–150CrossRefGoogle Scholar
  64. Rhumbler L (1911) Die Foraminiferen (Thalamophoren) der Plankton Expedition. Zugleich Entwurf eines natuerlichen Systems der Foraminiferen auf Grund selektonischer und mechanisch-physiologischer Faktoren. Erste Teil, Die allgemeinen Organizationsverhaltnisse der Foraminiferen. Ergebnisse der Plankton-Expedition der Humboldt Stiftung. von Lipsius & Tischer, Kiel und LeipzigGoogle Scholar
  65. Schiebel R (1992) Rezente benthische Foraminiferen in Sedimenten des Schelfes und oberen Kontinentalhanges im Golf von Guinea (Westafrika). Ber Geol-Paläontol Inst Univ Kiel 51:1–126, tables I–XII, pls 1–8Google Scholar
  66. Schmiedl G, Mackensen A, Müller PJ (1997) Recent benthic foraminifera from the eastern South Atlantic Ocean: dependence on food supply and water masses. Mar Micropaleontol 32:249–287CrossRefGoogle Scholar
  67. Schröder CJ (1986) Deep-water arenaceous foraminifera in the northwest Atlantic Ocean. Can Tech Rep Hydrogr Ocean Sci 71:1–191Google Scholar
  68. Schröder CJ, Scott DB, Medioli FS, Bernstein BB, Hessler RR (1988) Larger agglutinated foraminifera: Comparison of assemblages from central North Pacific and western North Atlantic (Nares Abyssal Plain). J Foramin Res 18:25–41CrossRefGoogle Scholar
  69. Schumacher S, Jorissen FJ, Dissard D, Larkin KE, Gooday AJ (2007) Live (Rose Bengal stained) and dead benthic foraminifera from the oxygen minimum zone of the Pakistan continental margin (Arabian Sea). Mar Micropaleontol 65:45–73CrossRefGoogle Scholar
  70. Scott DB, Franco SM, Schafer CT (2001) Monitoring in coastal environments using foraminifera and thecamobian indicators. Cambridge University Press, Cambridge Google Scholar
  71. Setty MGAP (1982) Recent marine microfauna from the continental margin, west coast of India. J Sci Ind Res India 41:674–679Google Scholar
  72. Setty MGAP, Nigam R (1982) Foraminiferal assemblages and organic carbon relationship in benthic marine ecosystem of western Indian continental shelf. Indian J Mar Sci 11:225–232Google Scholar
  73. Timm S (1992) Rezente Tiefsee-Benthosforaminiferen aus Oberflächensedimenten des Golfes von Guinea (Westafrika) - Taxonomie, Verbreitung, Ökologie und Korngrößenfraktionen. Ber Geol-Paläontol Inst Univ Kiel 59:1–155Google Scholar
  74. Todo Y, Kitazato H, Hashimoto J, Gooday AJ (2005) Simple foraminifera flourish at the ocean’s deepest point. Science 307:689Google Scholar
  75. Walton WR (1952) Techniques for recognition of living foraminifera. Contrib Cushman Found Foramin Res 3:56–60Google Scholar
  76. Wyrtki K (1973) Physical oceanography of the Indian Ocean: The Biology of the Indian Ocean. Springer, BerlinGoogle Scholar
  77. Zheng S, Fu Z (2001) Fauna Sinica; Phylum Granuloreticulosa, Class Foraminifera, Agglutinated Foraminifera. Science Press, Beijing, ChinaGoogle Scholar
  78. Zobel B (1973) Biostratigraphische Untersuchungen an Sedimenten des indisch-pakistanischen Kontinentalrandes (Arabisches Meer). ‘Meteor’ Forsch-Ergeb C 12:9–73Google Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.National Oceanography Centre SouthamptonSouthamptonUK
  2. 2.Biological Sciences Department Royal Holloway University of LondonEghamUK

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