Ecological and Biological Response of Benthic Foraminifera Under Oxygen-Depleted Conditions: Evidence from Laboratory Approaches
Abstract
Laboratory experiments are a valuable way to elucidate physiological and ecological processes of benthic foraminifera under oxygen-depleted conditions. Experimentally tested survival rates and other experiments show high tolerance of many species under low oxic to anoxic conditions. Laboratory observations raised different assumptions to explain the physiological adaptations to this tolerance. Denitrification processes seem to be one important mechanism. Nevertheless, foraminifera try to colonize sediment horizons with optimal species-specific oxygen concentrations. Experimental settings demonstrated the importance of oxygen gradients for the orientation in sediments. At the same time, foraminifera change the oxygen concentration in their microenvironment by respiration. Despite high bioturbation, they do not appear to influence the flux of oxygen into the sediment. Experimental working in oxygen-depleted environments needs a reliable determination of living foraminifera during the experiment, e.g., different biochemical techniques. Additionally, electrochemical or optical oxygen sensors that measure the oxygen concentration are necessary.
Keywords
Anoxic Condition Benthic Foraminifera Rose Bengal Foraminiferal Assemblage Facultative AnaerobeReferences
- Aller RC (1982) The effects of macrobenthos on chemical properties of marine sediment and overlying water. In: McCall PL, Tevesz MJS (eds) Animal-sediment relations. Plenum Press, New York, pp 53–102Google Scholar
- Alve E, Bernhard JM (1995) Vertical migratory response of benthic foraminifera to controlled oxygen concentrations in an experimental mesocosm. Mar Ecol Prog Ser 116:137–151CrossRefGoogle Scholar
- Arnold ZM (1954) Culture methods in the study of living foraminifera. J Paleontol 28:404–416Google Scholar
- Barmawidijaja DM, Jorissen FJ, Puskaric S, Van der Zwaan GJ (1992) Microhabitat selection by benthic foraminifera in the northern Adriatic Sea. J Foramin Res 22:297–317CrossRefGoogle Scholar
- Bernhard JM (1988) Postmortem vital staining in benthic foraminifera: duration and importance in population and distributional studies. J Foramin Res 18:143–146CrossRefGoogle Scholar
- Bernhard JM (1989) The distribution of benthic foraminifera with respect to oxygen concentrations and organic carbon levels in shallow-water Antarctic sediments. Limnol Oceanogr 34:1131–1141CrossRefGoogle Scholar
- Bernhard JM (1992) Benthic foraminiferal distribution and biomass related to pore-water oxygen content: central California continental slope and rise. Deep-Sea Res 39:585–605CrossRefGoogle Scholar
- Bernhard JM (1993) Experimental and field evidence of Antarctic foraminiferal tolerance to anoxia and hydrogen sulfide. Mar Micropaleontol 20:203–213CrossRefGoogle Scholar
- Bernhard JM (1996) Microaerophilic and facultative anaerobic benthic foraminifera: a review of experimental and ultrastructural evidence. Rev Paléobiol 15:261–275Google Scholar
- Bernhard JM (2000) Distinguishing live from dead foraminifera: methods review and proper applications. Micropaleontology 46:38–46Google Scholar
- Bernhard JM (2003) Potential symbionts in bathyal foraminifera. Science 299:861PubMedCrossRefGoogle Scholar
- Bernhard JM, Alve E (1996) Survival, ATP pool, and ultrastructural characterization of foraminifera from Drammensfjord (Norway): response to anoxia. Mar Micropaleontol 28:5–17CrossRefGoogle Scholar
- Bernhard JM, Bowser S (1999) Benthic foraminifera of dysoxic sediments: chloroplast sequestration and functional morphology. Earth-Sci Rev 46:149–165CrossRefGoogle Scholar
- Bernhard JM, Bowser S (2008) Peroxisome proliferation in foraminifera inhabiting the chemocline: an adaptation to reactive oxygen species exposure? J Eukaryot Microbiol 55:135–144PubMedCrossRefGoogle Scholar
- Bernhard JM, Reimers CE (1991) Benthic foraminiferal population fluctuations related to anoxia. Santa Barbara Basin, U.S. Pacific continental margin. J Foramin Res 27:301–310CrossRefGoogle Scholar
- Bernhard JM, Sen Gupta BK (1999) Foraminifera of oxygen-depleted environments. In: Sen Gupta BK (ed) Modern foraminifera. Kluwer Academic Publishers, Dordrecht, pp 201–216Google Scholar
- Bernhard JM, Newkirk SG, Bowser SS (1995) Towards a nonterminal viability assay for foraminiferan protists. J Eukaryot Microbiol 42:357–367CrossRefGoogle Scholar
- Bernhard JM, Buck KR, Barry JP (2001) Monterey Bay cold-seep biota: assemblages, abundance, and ultrastructure of living foraminifera. Deep Sea Res Pt I 48:2233–2249CrossRefGoogle Scholar
- 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:G03002CrossRefGoogle Scholar
- Bernhard JM, Barry JP, Buck KR, Starczak VR (2009) Impact of intentionally injected carbon dioxide hydrate on deep-sea benthic foraminiferal survival. Glob Change Biol 15:2078–2088CrossRefGoogle Scholar
- Borrelli C, Sabbatini A, Luna GM, Morigi C, Danovaro R, Negri A (2010) Determination of the metabolically active fraction of benthic foraminifera by means of fluorescent in situ hybridization (FISH). Biogeosciences Discuss 7:7475–7503CrossRefGoogle Scholar
- Bradshaw JS (1955) Preliminary laboratory experiments on ecology of foraminiferal populations. Micropaleontology 1:351–358CrossRefGoogle Scholar
- Bradshaw JS (1957) Laboratory studies on the rate of growth of the foraminifer, “Streblus beccarii (Linné) var. tepida (Cushman)”. J Paleontol 31:1138–1147Google Scholar
- Cedhagen T (1991) Retention of chloroplasts and bathymetric distribution in the sublittoral foraminiferan Nonionella labradorica. Ophelia 37:17–30Google Scholar
- Cedhagen T (1993) Taxonomy and biology of Pelosina arborescens with comparative notes on Astrorhiza limicola (Foraminiferida). Ophelia 37:143–162Google Scholar
- Corliss BH, Emerson S (1990) Distribution of Rose Bengal stained deep-sea benthic foraminifera from the Nova Scotian continental margin and Gulf of Maine. Deep-Sea Res 37:381–400CrossRefGoogle Scholar
- Delaca TE (1986) Determination of benthic rhizopod biomass using ATP analyses. J Foramin Res 16:285–292CrossRefGoogle Scholar
- Duijnstee IAP, Ernst SR, van der Zwaan GJ (2003) Effect of anoxia on the vertical migration of benthic foraminifera. Mar Ecol Prog Ser 246:85–94CrossRefGoogle Scholar
- Ernst S, Van der Zwaan B (2004) Effects of experimentally induced raised levels of organic carbon flux and oxygen depletion on a continental slope benthic foraminiferal community. Deep-Sea Res Pt I 51:1709–1739Google Scholar
- Forster S, Graf G (1992) Continuously measured changes in redox potential influenced by oxygen penetrating from burrows of Callianassy subterranea. Hydrobiologia 235(236):527–532CrossRefGoogle Scholar
- Forster S, Graf G (1995) Impact of irrigation on oxygen flux into the sediment: intermittent pumping by Callianassa subterranea and “piston-pumping” by Lanice conchilega. Mar Biol 123:335–346CrossRefGoogle Scholar
- Geslin E, Köhler-Rink S, Franke U, Heinz P, Holst G, Hemleben Ch (2002) Two dimensional oxygen distribution in sediment containing benthic foraminifers: laboratory study using planar optodes. In: Revets SA (ed) Forams 2002, volume of abstracts. University of Western Australia, PerthGoogle Scholar
- Geslin E, Heinz P, Jorissen F, Hemleben Ch (2004) Migratory responses of deep-sea benthic foraminifera to variable oxygen conditions: laboratory investigations. Mar Micropaleontol 53:227–243CrossRefGoogle Scholar
- Geslin E, Risgaard-Petersen N, Lombard F, Metzger E, Langlet D, Jorissen F (2011) Respiration rates of benthic foraminifera as measured with oxygen microsensors. J Exp Mar Biol Ecol 396:108–114CrossRefGoogle Scholar
- Gooday AJ (1986) Meiofaunal foraminiferans from the bathyal Porcupine Seabight (northeast Atlantic): size structure, standing stock, taxonomic composition, species diversity and vertical distribution in the sediment. Deep-Sea Res 33:1345–1373CrossRefGoogle Scholar
- Gross O (2000) Influence of temperature, oxygen and food availability on the migrational activity of bathyal benthic foraminifera: evidence by microcosm experiments. Hydrobiologica 426:123–137CrossRefGoogle Scholar
- Gross O (2002) Sediment interactions of foraminifera: implications for food degradation and bioturbation processes. J Foramin Res 32:414–424CrossRefGoogle Scholar
- Hannah F, Rogerson A (1997) The temporal and spatial distribution of foraminiferans in marine benthic sediments of the Clyde Sea area, Scotland. Estuar Coast Shelf Sci 44:377–383CrossRefGoogle Scholar
- Hannah F, Rogerson A, Laybourn-Parry J (1994) Respiration rates and biovolumes of common benthic foraminifera (protozoa). J Mar Biol Assoc U K 74:301–312CrossRefGoogle Scholar
- Heinz P (2001) Laboratory feeding experiments: response of deep-sea benthic foraminifera to simulated phytoplankton pulses. Rev Paléobiol 20:643–646Google Scholar
- Heinz P, Kitazato H, Schmiedl G, Hemleben Ch (2001) Response of deep-sea benthic foraminifera from the Mediterranean Sea to simulated phytoplankton pulses under laboratory conditions. J Foramin Res 31:210–227CrossRefGoogle Scholar
- Heinz P, Hemleben Ch, Kitazato H (2002) Time-response of cultured deep-sea benthic foraminifera to different algal diets. Deep-Sea Res Pt I 49:517–737CrossRefGoogle Scholar
- Heinz P, Geslin E, Hemleben Ch (2005) Laboratory observations of benthic foraminiferal cysts. Mar Biol Res 1:149–159CrossRefGoogle Scholar
- Heip CHR, Duineveld G, Flach E, Graf G, Helder W, Herman PMJ, Lavaleye M, Middelburg JJ, Pfannkuche O, Soetaert K, Soltwedel T, de Stigter H, Thomsen L, Vanaverbeke J, de Wilde P (2001) The role of the benthic biota in sedimentary metabolism and sediment-water exchange processes in the Goban Spur area (NE Atlantic). Deep-Sea Res Pt II 48:3223–3243CrossRefGoogle Scholar
- Hemleben C, Kitazato H (1995) Deep-sea foraminifera under long time observation in the laboratory. Deep-Sea Res 42:827–832CrossRefGoogle Scholar
- Høgslund S, Revsbech NP, Cedhagen T, Nielsen LP, Gallardo VA (2008) Denitrification, nitrate turnover, and aerobic respiration of benthic foraminiferans in the oxygen minimum zone off Chile. J Exp Mar Biol Ecol 359:85–91CrossRefGoogle Scholar
- Holst G, Grunwald B (2001) Luminescence lifetime imaging with transparent oxygen optodes. Sensor Actuator B 74:78–90CrossRefGoogle Scholar
- Holst G, Kohls O, Klimant I, König B, Kühl M, Richter T (1998) A modular luminescence lifetime imaging system for mapping oxygen distribution in biological samples. Sensor Actuator B 51:163–170CrossRefGoogle Scholar
- Jannink NT, Zachariasse WJ, Van der Zwaan GJ (1998) Living (Rose Bengal stained) benthic foraminifera from the Pakistan continental margin (northern Arabian Sea). Deep-Sea Res Pt I 45:1483–1513CrossRefGoogle Scholar
- Jorissen F (1999) Benthic foraminiferal microhabitats below the sediment-water interface. In: Sen Gupta BK (ed) Modern foraminifera. Kluwer Academic Publishers, Dordrecht, pp 161–179Google Scholar
- Jorissen FJ, De Stigter HC, Widmark JGV (1995) A conceptual model explaining benthic foraminiferal microhabitats. Mar Micropaleontol 26:3–15CrossRefGoogle Scholar
- Jorissen FJ, Wittling I, Peypouquet JP, Rabouille C, Relexans JC (1998) Live benthic foraminiferal faunas off Cape Blanc, NW-Africa: community structure and microhabitats. Deep-Sea Res Pt I 45:2157–2188CrossRefGoogle Scholar
- Josefson AB, Widbom B (1988) Differential response of benthic macrofauna and meiofaunal to hypoxia in the Gullmar fjord basin. Mar Biol 100:31–40CrossRefGoogle Scholar
- Kitazato H, Ohga T (1995) Seasonal changes in deep-sea benthic foraminiferal populations: results of long-term observations at Sagami Bay, Japan. In: Sakai H, Nozaki Y (eds) Biogeochemical processes and ocean flux in the Western Pacific. Terra Scientific Publishing Company, Tokyo, pp 331–342Google Scholar
- Kitazato H, Tsuchiya M (1999) Why are foraminifera useful proxies for modern and ancient marine environments? An example using Ammonia beccarii (LINNE) from brackish bay environments. Kagoshima University Research Center for the Pacific Islands, Occasional Papers 32:3–17Google Scholar
- Koho K, Piña-Ochoa E, Geslin E, Risgaard-Petersen N (2011) Survival and nitrate uptake mechanisms of foraminifers (Globobulimina turgida): laboratory experiments. FEMS Microbiol Ecol 75:273–283PubMedCrossRefGoogle Scholar
- Langer MR, Gehring CA (1993) Bacterial farming: a possible feeding strategy of some smaller, motile formainifera. J Foramin Res 23:40–46CrossRefGoogle Scholar
- Lee JJ, Muller WA (1973) Trophic dynamics and niches of salt marsh foraminifera. Am Zool 13:215–223Google Scholar
- Leutenegger S (1984) Symbiosis in benthic foraminifera: specificity and host adaptations. J Foramin Res 14:16–35CrossRefGoogle Scholar
- Meyers MB, Powell EN, Fossing H (1988) Movement of oxybiotic and thiobiotic meiofauna in response to changes in pore-water oxygen and sulfide gradients around macro-infaunal tubes. Mar Biol 98:395–414CrossRefGoogle Scholar
- Moodley L, Hess C (1992) Tolerance of infaunal benthic foraminifera for low and high oxygen concentrations. Biol Bull 183:94–98CrossRefGoogle Scholar
- Moodley L, Van der Zwaan GJ, Herman PMJ, Kempers L, van Breugel P (1997) Differential response of benthic meiofaunal to anoxia with special reference to foraminifera (Protista: Sarcodina). Mar Ecol Prog Ser 158:151–163CrossRefGoogle Scholar
- Moodley L, Schaub BEM, Van der Zwaan GJ, Herman PMJ (1998a) Tolerance of benthic foraminifera (Protista: Sarcodina) to hydrogen sulphide. Mar Ecol Prog Ser 169:77–86CrossRefGoogle Scholar
- Moodley L, Van der Zwaan GJ, Rutten GMW, Boom RCE, Kempers AJ (1998b) Subsurface activity of benthic foraminifera in relation to porewater oxygen content: laboratory experiments. Mar Micropaleontol 34:91–106CrossRefGoogle Scholar
- Moodley L, Steyaert M, Epping E, Middelburg JJ, Vincx M, van Avesaath P, Moens T, Soetaert K (2008) Biomass-specific respiration rates of benthic meiofauna: demonstrating a novel oxygen micro-respiration system. J Exp Mar Biol Ecol 357:41–47CrossRefGoogle Scholar
- Morigi C, Geslin E (2009) Quantification of benthic foraminiferal abundance. In: Danovaro R (ed) Methods for the study of deep-sea sediments, their functioning and biodiversity (from viruses to megafauna). CRC Press, Boca RatonGoogle Scholar
- Mortimer RJG, Davey JT, Krom MD, Watson PG, Frickers PE, Clifton RJ (1999) The effect of macrofauna on porewater profiles and nutrient fluxes in the intertidal zones of the Humber Estuary. Estuar Coastal Shelf Sci 48:683–699CrossRefGoogle Scholar
- Muller WA, Lee JJ (1969) Apparent indispensability of bacteria in foraminiferan nutrition. J Protozool 16:471–478Google Scholar
- Murray JW (1963) Ecological experiments on foraminiferida. J Mar Biol Assoc UK 43:621–642CrossRefGoogle Scholar
- Murray JW (ed) (2006) Ecology and applications of benthic foraminifera. Cambridge University Press, CambridgeGoogle Scholar
- Nomaki H, Heinz P, Hemleben Ch, Kitazato H (2005) Behavior and response of deep-sea benthic foraminifera to freshly supplied organic matter: a laboratory feeding experiment in microcosm environments. J Foramin Res 35:103–113CrossRefGoogle Scholar
- Nomaki H, Yamaoka A, Shirayama Y, Kitazato H (2007) Deep-sea benthic foraminiferal respiration rates measured under laboratory conditions. J Foramin Res 37:281–286CrossRefGoogle Scholar
- Nyholm K-G, Nyholm P-G (1975) Ultrastructure of monothalamous foraminifera. Zoon 2:117–122Google Scholar
- Ohga T, Kitazato H (1997) Seasonal changes in bathyal foraminiferal populations in response to the flux of organic matter (Sagami Bay, Japan). Terra Nova 9:33–37CrossRefGoogle Scholar
- Panchang R, Nigam R, Linshy V, Rana SS, Ingole B (2006) Effect of oxygen manipulations on benthic foraminifera from Central West Coast of India: a preliminary laboratory experiment. Indian J Mar Sci 35:235–239Google Scholar
- Piña-Ochoa E, Høgslund S, Geslin E, Cedhagen T, Revsbech NP, Nielsen LP, Schweizer M, Jorissen F, Rysgaard S, Risgaard-Petersen N (2010a) Widespread occurrence of nitrate storage and denitrification among foraminifera and gromiids. Proc Natl Acad Sci 107:1148–1153PubMedCrossRefGoogle Scholar
- Piña-Ochoa E, Koho K, Geslin E, Risgaard-Petersen N (2010b) Survival and life strategy of foraminifer, Globobulimina turgida, through nitrate storage and denitrification: laboratory experiments. Mar Ecol Prog Ser 417:39–49CrossRefGoogle Scholar
- Pucci F, Geslin E, Barras C, Morigi C, Sabbatini A, Negri A, Jorissen F (2009) Survival of benthic foraminifera under hypoxic conditions: results of an experimental study using the cell tracker green method. Mar Pollut Bull 59:336–351PubMedCrossRefGoogle Scholar
- Risgaard-Petersen N, Langezaal AM, Ingvardsen S, Schmid MC, Jeten MSM, Ob den Camp HJM, Derksen JWM, Piña-Ochoa E, Eriksson SP, Nielsen LP, Revsbech NP, Cedhagen T, Van der Zwaan GJ (2006) Evidence for complete denitrification in a benthic foraminifer. Nature 443:93–96PubMedCrossRefGoogle Scholar
- Schmiedl G, Mitschele A, Beck S, Emeis K-C, Hemleben C, Schulz H, Sperling M, Weldeab S (2003) Benthic foraminiferal record of ecosystem variability in the eastern Mediterranean Sea during times of sapropel S5 and S6 deposition. Paleogr Paleoclim Paleoecol 190:139–164CrossRefGoogle Scholar
- 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 62:45–73CrossRefGoogle Scholar
- Sen Gupta BK, Machain-Castillo ML (1993) Benthic foraminifera in oxygen-poor habitats. Mar Micropaleontol 20:183–201CrossRefGoogle Scholar
- Szarek R, Nomaki H, Kitazato H (2007) Living deep-sea benthic foraminifera from the warm and oxygen-depleted environment of the Sulu Sea. Deep-Sea Res II 54:145–176CrossRefGoogle Scholar
- Travis JL, Bowser SS (1991) The mobility of Foraminifera. In: Lee JJ, Anderson OR (eds) Biology of the foraminifera. Academic, London, pp 91–155Google Scholar
- Travis JL, Browser SS (1986) Microtubule-dependent reticulopodial motility: is there a role for actin? Cell Motil Cytoskeleton 6:2–14PubMedCrossRefGoogle Scholar
- Vachard D, Pille L, Gaillot J (2010) Palaeozoic foraminifera: systematics, palaeoecology and responses to global changes. Rev Micropal 53:209–254CrossRefGoogle Scholar