Respiration in the dark ocean

GEOPHYSICAL RESEARCH LETTERS, VOL. 30, NO. 2,1041, doi:IO.1029/2002GLOJ6227, 2003 Respiration in the dark ocean Javier Aristegui Facultad de Ciencias del ~ar, Universidad de las Palmas de Gran Canaria, Spain Susana Agustí and Carlos M. Duarte IMEDEA (CS1C-UIB), Instituto Mediterráneo de Estudios Avanzados, Spain Received 5 September 2002: accepted 28 October 2002: published 18 January 2003. [1] The dark ocean, the waters below 200 rn dep~h, 2. Methods comprises about 95% of the volume of the ocean, but Its [3] Direct estimates of microplankton respiratory activcontribution to the metabolism of the acean is poorly ity through oxygen consumption in the dark ocean are quantified. Rere we show that the respiration rate of only available from the Oulf of México [Biddallda and microplankton declines exponentially at arate of 0.53 km -1 Benner, 1997J, a highly eutrophic region which does not \i\ \\\e dü!~ ocea\'\., 0.\\<1 \",'en\\üw:ed at t\\e "!'.tenace betweeu represent open ocean concú"úons \'la'o)e \J. 'í'ne 'oui'K t6 the mesopelagic and the abyssal layers (1,000-2,O~0 m). the available estimates were derived from measurements of The respiratory CO2 productian in the dark ocean, estlmated the respiratory eleclron transport system (ETS) activity. On at 20 to 33.3 Gt e yrI, renders it a major component of the contrary to the oxygen method, the ETS approach the carbon flux in the biosohere. INDEX TERMS: 4805 allows the collection of large data sets during field cruises, Oceanography: Biological and Chemical: Biogeochemical cycles facilitating the extension of our knowledge of oceanic (1615); 4806 Oceanography: Biological and Chemieal: Carbon respiration over large temporal. and spatial scal~s: The cycling; 4850 Oceanography: Biologieal and Chemical: Organic ETS method estimates the maxm1Um overalI actlv¡ty of marine chemistry; 4855 Oceanography: Biological and Chemical: the enzymes associated with the respiratory electron transPlankton. Citation: Arístegui, J., S. Agustí, and C. M. Duarte, port system under substrate saturation, in both eukaryotic Respiration in the dark oeean, Geophys. Res. Lell., 30(2), 1041, and prokaryotic organisms. ETS activity measurements doi: 1 0.1 029120020LO 16227, 2003. represent, therefore, potentíal respiration ra~es. These were 1. Introduction [2J Recent revision of the respiratory activity of microplankton as a major source OfC02 in the ocean has focussed on the mixed layer, comprising the top 200 m of che ocean ¡Duarte and AguslÍ, 1998; Williams, 1998; Duarle el al., 2001]. Although this layer supports intense metabolic processes it represent <5% of the volume of the ocean. The dark ocean, the waters below 200 ro depth, represents the main reservoir of organic carbon [Field el al., 1998J and an important component of the carbon cycle, throu~h tbe remineralisation of organic matter [Ducklow, 1995J, In the ocean. Yet, the estimation of the respiratory activity in tne car'K oeean 15 cum'oen,ome O\le lO \.'ne \o'W !ale'io \'ne ... e\ .... , about !O to lOO-fold lower than those in the photic layer [Packard el al., 1988; Biddanda and Benner, 1997], and has, therefore, received little attention. As a consequence, the total e flux involved has only bec:1 assessed indirectly, as the difference between the export af organic carbon from the mixed layer and the burial of organic carbon in the ocean floor. However, these estimates range by an order of magnitude [Sambrotto el al., 199 . 3; ~alkowski el al., 1?98; Louanchi alld Najjar, 2000J, indICatmg that the magmtude of respiration in the dark ocean is poorly constrained by stlch indirect estimates. We, therefore, compiled available estimates of respiratory activity in the dark ocean (Table 1) to attempt a ó'Hect asse5sment 01 \'ne g\o"ua\ 1:e<,;?\~\.\\)~ ,a\.e there. Copyright 2003 by the American Gcophysical Unil'n. 0094-8276/03/2002GLO 16227505.00 con verted to actual respiratory rates usmg a constant (0.086) der¡ved from emp'nica) re)aÍlons'rÍlps w'rtn oxygen consumption rates determined in vitro trom monospecific cultures of bacteria [Chrislensen el al., 1980]. These estimates involve an error of ±30% [Packard el al., 198B]. In essence, the derivation assum~s an ave~a!!e relationship between enzyme mass and resplratory actlvlty applieable to bacterial communities, independently of depth, temperature, geographic loeation and other local conditions. Such an assumption introduces uncertainty On these estimates that can only be assesed through future validation. Hence, calculated respiration rates must be interpreted with some degree of caution. 3. Results and Discussion [4) The available estimates of areal respiration in the dark oeean (200 In to ocean tloor) indicate rates in the ordcr of about 5 mol C m -2 yrI, or abaut 20 Ot C yrI over the global dark ocean, being in clase agreement with oxygen utilization rates inferred from large-scalc tracer balances [Jenkins, 1982; JeJlkills al~d Wallace, 19~2) and other biogeochemical tracer techmques for deterrmnmg the total new production [Carlson el al. , 1994). [sJ Most profiles of respiration rates indicate an expo~ nential decline in respiration rates with increasing depth, with rates averaging 0.56 km -1 for the different sites exam'meo ~'ía'o\e \). Tnc eS'úmaÚtm Dí' 'j)'t i.Du:.\ 't'e"¡¡?1Th\)D1'1 in the global dark ocean by up-scaling ftom the pub1ished area! rates is suboptimal, due to the differential integratiol1 depths used in the various studies (Table 1). Improved estimates can be derived from the depth-dependence of respiration rates, which decline exponentiaHy with inereas" 13 -1 13 -2 ARÍSTEGUI ET AL.: RESPIRATION IN THE DARK OCEAN Table 1. Areal Estimates of Microplankton Respiration (R) in the Dark Ocean Oeean D!:J1th range ím) R ímolC m2 ~r-I) N stations Method Atlantic (Sargasso Sea)" 200-1000 3.3 AOU/ttacers Atlantic (Sargasso Sea)b 200-1000 1.5 8 ETS 1000-bottom 0.7 8 ETS Atlantic (west IberiaIMorocco)C 200-1500 6.9 1 ETS Atlaotic (meddies)" 200-1500 6.1 2 ETS Atlantic (Canaty Islands)d 200-1000 2.4 11 ETS Atlantic (Gulf of Mexico)" 100-500 118 .1 7 Winkler Mediterranean (westt 200-1500 6.8 2 ETS Mediterranean (west)f 200-3000 1.3 8 ETS Mediterranean (west)8 200-800 2.2 24 ETS Mediterranean (westt 200-1000 1.2 10 ETS Mediterranean (east)' 200-3000 4.3 >10 ETS Indian Ocean (Arabian ScaY . 200-2400 5.2 6 ETS Indian Ocean (Bay of BengalY 200-2400 2.2 6 ETS Pacific Occan (Guinea Dome)b 200-1000 3.9 >15 ETS 1000-bottom 2.6 >4 ETS Southem Ocean (Indian sector)k 200-1000 1.5 7 ETS ETS = Respiratory Electron TrilOsport System activity; Winkler= Winkler oxygen determinatíon; AOU/tracers = estimates from oxygen fields and water mass age. 'Jenkins and Waliace, 1992. bpackard el al., 1988. cSavenkc.fJ el al., 1993a. dJ. Arislegui, unpublished data. cBiddaTUÚl and Benner, 1997 . fClzrislensen el aL, 1989. sSavenko.fJ el al., 1993 b. hLefevre el al., 1996. ;Lo Feria and Azzaro, 2001. iNaqvi et al., 1996. kAristegui et al., 2002. ing depth (Z, Figurela), as described by the fitted regression equation R (¡.unol O2 m -3 d -1) == 18.0 e -0 .53 Z (Km) (R 2 == 0.760, F == 73.6, P < 0.00001). Inspection of the residuals showed an enhanced respiratory activity at 1,000-2,000 m depth, corresponding to the base of the pennanent thennocline separating the mesopelagic from the abyssal layers, relative to that expected from tbe general decline in respíratory activity with depth (Figure lb). Examination of the individual profiJes (TabJe 1) showed the enhanced respiratory activity to be a consistent feature in various seas and oceans, rather than an anomaly of a particular basin. The origin of these enhanecements remains unclear, but may derive from mixing of water masses at the base of the 1 10 100 o 1000 E 2000 --- .J::. -3000 a. OJ o <1000 • • 5000 • • a 6000 L_____ -'- _____ -' thermocIine, or may be produced in situ by migrant zooplankton. [6] These resu1ts indicate that 50% of the microplankton respiration within the dark ocean occurs between 200 and 700 m depth, and that 90% ofthe microplankton respiration within the dark ocean occurs between 200 and 4,500 m (Figure 2). The integration of the depth-averaged estimates of microplankton respiration in the dark ocean (Figure 1) using the percentage of the ocean surface comprised within the different depth zones [Menard and Smith, 1966], yielded an estimate oftotal respiration in the dark ocean of33.3 Ot e yr-I, pointing to microplankton respiration in the dark ocean as a major source of CO2• This estimate must be Residual R (IJmol 02 m-'l dO') .a -4 ·2 o 2 4 6 8 10 12 o 1000 o 2000 ro "O - :J' 3000 ,.... 3 - 4000 500() b GOOO Figure 1. The depth distribution of the average (±SE) respiration rate in the dark ocean (a) and the depth distribution of the residuals from the fitted exponentiaI equation (h). Rates compiled from references in Table l. ARÍSTEGUI ET AL.: RESPIRATION IN TI-IE DARK OCEAN 13 • 3 Fractional Cumulative Respiration estimates, traditionaIly based on particulate export were expanded to inc1ude export of dissolved organic carbon as 0.0 0.2 DA 0.6 0.8 O 1.0 well [Car/son et a/., 1994]. Indeed, it has recently been r---r-....,.....-.---r--.--r---r--,---r---,. suggested that sediment traps may severely underestimate * • -------~1.1 1* 1000 1*; .... ."I+l I '~=- • .:;.~ " I E 2000 '.~ '-' I .c: ~ I - Q.. 3000 Ht...., I (J,) I Cl ~--i I 4000 • I ~~ I 5000 .' I I I • ¡ l 6000 Figure 2. The depth distribution of the average (±SE) cumulative respiration rate in the dark ocean. Rates compiled from references in Table l. Dotted lines indicate depths comprising 50% and 10% of the water colunm respiration in the dark ocean. regarded as a first approximation, because the data set available (Table 1) is unbalanced in the depth and geographical distribution. Although the 200-2,000 m layer is covered by a significant (N = 600) empirical base, that between 2,000 and the ocean floor is stiII meager (N = 25). The geographical spread of the data is also dominated by estimates from the Atlantic and the Mediterranean Seas. However, the estimates available suggest limited geographical variability in the rates observed in the dark ocean (Table 1), particularly those in the abyssal waters (Figure 1 a), so that the estímate of 33.3 Gt C yr-J is proposed to be índicative of the bulk figure contributed by microplankton respiration in the dark ocean. [7] The estimates ofrespiration in the dark oeean derived here do not in elude respiration by metazoans, which may contribute a significant percentage of the total respiration in the dark oeean [Longhurst el al., 1990], nor benthic respiration, which is believed to add about 0.8 Gt C yrI [Jahnke, 1996]. Hence, although the estimates of respiration in the dark ocean, ranging between 20 Gt e yrJ, derived from the areal rates, and 33.3 Gt e yrI, derived from the depth-distribution of the rates, may seem high, they should be considered to be conservative. [8] The respiration in the dark oeean has been inferred indireetly in the past from the estimated organie carbon inputs to the dark ocean. The total organic carbon exported from the photic layer ofthe ocean is estimated at 15-16 Gt e yrJ [Sambrotto et al., 1993; Falkowski el al., 1998], but do es not inelude active transport of organie matter by mesozooplankton, lateral inputs from the shelf, estimated at about 2 Gt C yearJ [Liu el al., 2000], nor organic matter produced by chemosynthesis in the dark ocean, the magnitude of which remains unknown. However, the estimates of the organic carbon inputs to the dark ocean have been steadily increasing in the past, partieularly since these the sinking particle flux [Michaels el al., 1994] This would partly explain the large discrepancies between particulate organic carbon flux and both benthic carbon remineralization in the deep ocean [Wenzhofer and G/ud, 2002] and export production inferred from geochemical tracers [Carlson el al., 1994; Michae/s el al., 1994]. Hence, the size of the organic carbon input to the dark ocean is still under revision. The estimates derived by up-scaling from ETSbased measurements provided here are, however, consistent with those derived using geochemical tracers [Jenkins, 1982; Jenkins and Wallace, 1992; Carlson el al., 1994). 4. Conclusions [9) In summary, the analysis presented here confim1s respíration ín the dark ocean to be a major component of the carbon cyc1e in the biosphere. The much lower vol umetric rates compared to those in the photic layer are compensated by the vastly larger volume of the dark ocean. This results in an estimated respiratory COz production in the dark ocean of20 to 33 Gt C yrJ, to which the enhanced microplankton respiration at the base of the permanent thermocline (1,000-2,000 m) has an important contri bution. These estimates help constrain present estimates of the inputs of organic carbon to the dark ocean, which are critical to establish the role ofthe biologieal pump in the removal of atmospheric CO2• In particular, the results presented should promote an improved understanding of the oceanic carbon cycle abre to accommodate the large respíratíon rates oceurring in the dark ocean. [10] Acknowledgments. We gratefuJly acknowledge Hugh Ducklow and one anonymous reviewer for valuable suggestions. Thanks also to Ted Packard for encouraging research on ETS. 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