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The Role of Benthic Foraminifera in the Benthic Nitrogen Cycle of The EGU Journal Logos (RGB) Open Access Open Access Open Access Advances in Annales Nonlinear Processes Geosciences Geophysicae in Geophysics Open Access Open Access Natural Hazards Natural Hazards and Earth System and Earth System Sciences Sciences Discussions Open Access Open Access Atmospheric Atmospheric Chemistry Chemistry and Physics and Physics Discussions Open Access Open Access Atmospheric Atmospheric Measurement Measurement Techniques Techniques Discussions Open Access Biogeosciences, 10, 4767–4783, 2013 Open Access www.biogeosciences.net/10/4767/2013/ Biogeosciences doi:10.5194/bg-10-4767-2013 Biogeosciences Discussions © Author(s) 2013. CC Attribution 3.0 License. Open Access Open Access Climate Climate of the Past of the Past Discussions The role of benthic foraminifera in the benthic nitrogen cycle of the Open Access Open Access Peruvian oxygen minimum zone Earth System Earth System Dynamics 1,2 2 2 2 1,* 2 Dynamics N. Glock , J. Schonfeld¨ , A. Eisenhauer , C. Hensen , J. Mallon , and S. Sommer Discussions 1Sonderforschungsbereich 754, Christian-Albrechts-University Kiel, Climate-Biogeochemistry Interactions in the Tropical Ocean, Kiel, Germany Open Access Open Access 2GEOMAR, Helmholtz-Zentrum fur¨ Ozeanforschung Kiel, Wischhofstr. 1–3, 24148 Kiel, GermanyGeoscientific Geoscientific *present address: Geoteam Schaffer, Gartnerstrasse¨ 38, 70329 Stuttgart, Gemany Instrumentation Instrumentation Methods and Methods and Correspondence to: N. Glock ([email protected]) Data Systems Data Systems Received: 4 December 2012 – Published in Biogeosciences Discuss.: 12 December 2012 Discussions Open Access Revised: 29 May 2013 – Accepted: 10 June 2013 – Published: 15 July 2013 Open Access Geoscientific Geoscientific Model Development Abstract. The discovery that foraminifera are able to use ni- ing benthic foraminiferaModel (3Development to 3955 µmol L−1) can be higher Discussions trate instead of oxygen as an electron acceptor for respiration by three orders of magnitude as compared to the ambient has challenged our understanding of nitrogen cycling in the pore waters in near-surface sediments sustaining an impor- Open Access ocean. It was thought before that only prokaryotes and some tant nitrate reservoir in Peruvian OMZ sediments.Open Access The sub- fungi are able to denitrify. Rate estimates of foraminiferal stantial contribution of foraminiferalHydrology nitrate and respiration to to- Hydrology and denitrification have been very sparse and limited to specific tal benthic nitrate loss atEarth the Peruvian System margin, which is one Earth System regions in the oceans, not comparing stations along a tran- of the main nitrate sink regions in the world ocean, underpins sect of a certain region. Here, we present estimates of ben- the importance of the previouslySciences underestimated role of ben- Sciences thic foraminiferal denitrification rates from six stations at in- thic foraminifera in global biogeochemical cycles. Discussions Open Access termediate water depths in and below the Peruvian oxygen Open Access minimum zone (OMZ). Foraminiferal denitrification rates Ocean Science were calculated from abundance and assemblage composi- Ocean Science Discussions tion of the total living fauna in both surface and subsurface 1 Introduction sediments, as well as from individual species specific den- itrification rates. A comparison with total benthic denitrifi- Nitrate is a limiting nutrient in surface ocean primary pro- Open Access Open Access cation rates as inferred by biogeochemical models revealed ductivity and takes a central role in marine biogeochem- that benthic foraminifera probably account for the total den- istry (Gruber, 2004; Arrigo, 2005; Lam et al., 2009). In the Solid Earth oceanic nitrogen cycle, N2 Solidfrom the Earth atmosphere becomes itrification in shelf sediments between 80 and 250 m water Discussions depth. The estimations also imply that foraminifera are still bioavailable by N2 fixation. The loss of nitrogen from the important denitrifiers in the centre of the OMZ around 320 m marine ecosystem to the atmosphere as N2 gas is domi- nated by two major pathways. One way is nitrate respiration (29–50 % of the benthic denitrification), but play only a mi- Open Access Open Access nor role at the lower OMZ boundary and below the OMZ in facultative anaerobic microorganisms which produce N2 from NO− (heterotrophic denitrification). The other process between 465 and 700 m (2–6 % of total benthic denitrifi- 3 The Cryosphere is anaerobic oxidationThe of ammonium Cryosphere (Anammox) by NO−, cation). Furthermore, foraminiferal denitrification has been 2 Discussions compared to the total benthic nitrate loss measured during which yields N2 (van de Graaf et al., 1995; Thamdrup and benthic chamber experiments. The estimated foraminiferal Dalsgaard, 2002; Kuypers et al., 2003). denitrification rates contribute 2 to 46 % to the total nitrate About 20 to 40 % of the global nitrogen loss in the loss across a depth transect from 80 to 700 m, respectively. oceans is estimated to take place in oxygen minimum zones Flux rate estimates range from 0.01 to 1.3 mmol m−2 d−1. (OMZs), although these zones occupy only 0.1 % of the Furthermore we show that the amount of nitrate stored in liv- global ocean volume (Gruber and Sarmiento, 1997; Gru- ber, 2004; Lam et al., 2009). Nitrate is usually depleted in Published by Copernicus Publications on behalf of the European Geosciences Union. 4768 N. Glock et al.: The role of foraminifera in the Peruvian OMZ’s benthic nitrogen cycle near-surface waters due to utilisation by primary produc- odes (Finlay et al., 1983). Prokopenko et al. (2011) showed ers. Remineralisation of degraded organic matter produces that denitrification in anoxic sediments is strongly supported + − NH4 which is stepwise oxidized to NO3 under aerobic by biological nitrate transport through cell-stored nitrate. − They also estimated based on a data constrained model that conditions (nitrification). Thus, the NO3 concentration usu- ally increases with water depth. Denitrification also proceeds at least 31 % of the total N2 production in anoxic sediments stepwise with a number of intermediate species involved is mediated by biologically transported nitrate. − → − → → → In order to estimate the contribution of foraminiferal deni- (NO3 NO2 NO N2O N2). Nevertheless, only the complete process with the final product N2 meets the strict trification to the total benthic denitrification and the total ben- definition of denitrification (Zumft, 1997; Lam et al., 2009). thic nitrate turnover in the Peruvian OMZ, we apply species- Another concurring nitrate consuming process is dissim- specific denitrification rates as documented in the literature ilatory nitrate reduction to ammonium (DNRA). It usually to living benthic foraminiferal assemblages at six sampling takes place under low-oxygen conditions. DNRA by sulfur stations. The results will emphasize the relevance of benthic bacteria (Thioploca and Beggiotoa) seems to be a major path- foraminifera for the nitrogen budget at one of the most im- way of nitrate loss at the shelf and upper slope of the Peru- portant nitrate sinks in the world ocean. vian OMZ between 78 and 259 m water depth, while denitri- fication is the major pathway at depths beyond 319–1005 m (Bohlen et al., 2011; Mosch et al., 2012). 2 Material and methods Recent studies showed that several benthic foraminiferal species facultatively may change to nitrate respiration when 2.1 Sampling procedure dissolved oxygen becomes depleted in the water (Risgaard- Petersen et al., 2006; Pina-Ochoa˜ et al., 2010a). Four of the During R/V Meteor cruises M77/1 and M77/2 (October and analysed foraminiferal species (all from Peruvian OMZ) den- November 2008), six sediment cores from the Peruvian OMZ itrify to N2O rather to N2, implying that they might lack ni- were recovered with a video-guided multiple corer (MUC) trous oxide reductase (Pina-Ochoa˜ et al., 2010a). The contri- for foraminiferal analyses in the present study (Fig. 1, Ta- bution of foraminiferal denitrification to the total nitrate loss ble 1). The coring tubes were of 100 mm inner diameter. may range from 4 % (Sagami Bay, Japan; Glud et al., 2009) Immediately after retrieval, one multicorer tube was brought ◦ to more than 70 % (Bay of Biscay or Skagerrak; Pina-Ochoa˜ to a cooling laboratory with a constant temperature of 4 C. et al., 2010a). Even if the contribution of foraminiferal deni- Supernatant water of the core was carefully removed. The trification is considered low like at the Sagami Bay study site, core was sliced in 2 or 5 mm intervals from 0 to 10 mm, − ∼ in 5 mm intervals from 10 to 40 mm, and in 10 mm inter- NO3 stored in foraminiferal cells still comprised 80 % of the total benthic nitrate pool. Results of Risgaard-Petersen et vals from 40 to 50 mm sediment depth in order to resolve al. (2006) and Bernhard et al. (2012a) suggested that deni- the microhabitat structure of endobenthic foraminifera (e.g. trification in Globobulimina pseudospinescens (Globobulim- Corliss, 1985; Bernhard et al., 2003).The samples were filled ina turgida of authors), Bolivina argentea, Fursenkoina cor- in PVC bottles, stained and preserved with a solution of 2 nuta and Nonionella stella is not performed by prokaryotic gram rose bengal per liter of ethanol (Lutze and Altenbach, symbionts. Even after treatment with antibiotics, B. argen- 1991; Schonfeld¨ et al., 2012). Afterwards, the samples were ◦ tea was still able to denitrify (Bernhard et al., 2012a). Nev- transported and then stored at 4 C at
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