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The oxygen minimum zone of the eastern South Pacific
ARTICLE IN PRESS Deep-Sea Research II 56 (2009) 987–991
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The oxygen minimum zone of the eastern South Pacific Osvaldo Ulloa , Silvio Pantoja ´fica en el Pacı´fico Sur-oriental, Universidad de Concepcio ´n Oceanogra ´n, Casilla 160-C, Concepcio ´n, Chile Departamento de Oceanografı´a and Centro de Investigacio
a r t i c l e in fo
abstract
Available online 10 December 2008
In spite of the fact that oxygen-deficient waters with p20 mM of dissolved oxygen—known as oxygen minimum zones (OMZs)—occupy only 1% of the volume of the global ocean, they disproportionately affect global biogeochemical cycles, particularly the nitrogen cycle. The macrobiota diversity in OMZs is low, but the fauna that do inhabit these regions present special adaptations to the low-oxygen conditions. Conversely, microbial communities in the OMZ water column and sediments are abundant and phylogenetically and metabolically very diverse, and microbial processes occurring therein (e.g., denitrification, anammox, and organic matter degradation) are important for global marine biogeochemical cycles. In this introductory article, we present the collection of papers for the special volume on the OMZ of the eastern South Pacific, one of the three main open-ocean oxygen-deficient regions of the global ocean. These papers deal with aspects of regional oceanography, inorganic and organic geochemistry, ecology, and the biochemistry of micro and macro organisms—both in the plankton and in the sediments—and past changes in the fish scales preserved in the sediments bathed by OMZ waters. & 2008 Elsevier Ltd. All rights reserved.
Keywords: Oxygen minimum zone Biogeochemical cycling Microbial communities Plankton Benthos Fish scales
1. Introduction Oxygen is a key element for biology and the cycling of geochemical elements, and has shaped the chemical and biological evolution on Earth. Oxygen accounts for 21% of the volume in the atmosphere and is the most thermodynamically favorable terminal electron acceptor for organic matter oxidation, making it the current main oxidant for the energetic demands of the biosphere. However, exceptions to this can be found in the soils, ocean sediments, anoxic water bodies, and certain compartments in living organisms (e.g., digestive tracks) that are restricted from a sufficient supply of dissolved oxygen to compensate for its lost by aerobic respiration. Because of the thermohaline circulation, oxygen penetrates the deepest waters of the global ocean, including the abyssal plains and trenches. However, due to the respiration of the organic matter produced in the lighted surface layer as it settles down through the water column and the nature of global deep circulation, the oxygen concentrations in intermediate waters (100–1000 m deep) are lower than in the surface waters above and deep waters below (Wyrtki, 1962). Moreover, in some regions, upwelling, sluggish circulation, and high primary productivity in surface waters cause oxygen concentrations in subsurface waters to drop to levels o20 mM and possibly even to anoxia; these permanently low-oxygen regions are known as oxygen minimum zones (OMZs). These features occur in large open-ocean areas of
the eastern tropical Pacific Ocean and the northern reaches of the tropical Indian Ocean (Kamykowski and Zentara, 1990). OMZ waters also impinge on the sea floor of continental margins (Helly and Levin, 2004). These areas have low biodiversity of macrofauna, and are inhospitable to most commercially valuable marine resources. However, OMZs support benthic communities that include conspicuously large sulfur-oxidizing bacteria, nitrate-respiring protists, and metazoans adapted to oxygen-deficient conditions (e.g., Gallardo, 1977; Levin, 2003; Risgaard-Petersen et al., 2006). In March 2002, the Chilean government established the Center for Oceanographic Research in the eastern South Pacific (Centro de Investigacio´n Oceanogra´fica en el Pacı´fico Sur-Oriental, COPAS) at the Universidad de Concepcio´n (http://www.copas.udec.cl) as one of the country’s centers of excellence (Lange and Ulloa, 2003). From the beginning, one of the main research themes at COPAS has been the study of the structure and functioning of the OMZ in the eastern South Pacific. Several articles on the topic have been published elsewhere (see references), as have sets of articles on the oceanographic characteristics of the region (Morales and Lange, 2004; Escribano and Schneider, 2007). A collection of new articles dealing with the study of the OMZ is presented in this issue. The following provides a brief overview of some of the major highlight of the articles published herein.
2. Large-scale features Corresponding author. Tel.: +56 41 220 3585; fax: +56 41 223 9900.
E-mail address: [email protected] (O. Ulloa). 0967-0645/$ - see front matter & 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2008.12.004
According to the World Ocean Atlas 2001 (WOA01), waters with p20 mM of dissolved oxygen represent only 1% of the
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volume of the global ocean, whereas waters with p10 mM account for o0.3% (Fig. 1). However, as shown by Fuenzalida et al. (2009), estimates based on the WOA01 product may severely underestimate (up to 90%) the volume and area of the OMZ in the eastern South Pacific Ocean. This is probably also the case for the other OMZs. Part of the problem lies in the density of data from the region that went into producing the WOA01. Another problem, as discussed by Fuenzalida et al., is the way in which the WOA01 are processed, using 33 standard depths to obtain the gridded climatologies versus the quasi-continuous modern data obtained with conductivity-temperature-depth-oxygen (CTDO) profilers. Apart from the low-oxygen concentrations, a characteristic feature of OMZs is the presence of an inorganic nitrogen (N) deficit relative to inorganic phosphorus (P). As organic matter produced at the surface with a relatively fixed ratio of nitrogen to phosphorus (the Redfield ratio) sinks and becomes mineralized, N and P are released in the same proportion, such that the concentrations of inorganic N and P in the ocean are close to the molar ratio in organic matter (16:1); this is the case in most of the global ocean. However, in OMZs, nitrogen is lost primarily as N2 through heterotrophic denitrification and anammox (see the next section), so that the concentration of inorganic nitrogen (mainly nitrate+nitrite) deviates significantly from the Redfield ratio and can be quantified as a nitrogen deficit. Silva et al. (2009) used historical data collected from 101 to 501S and from the South American west coast to 1001W to describe the main physical and chemical characteristics of the water masses in the region. They also used the nitrate deficit as chemical marker to trace Equatorial Subsurface Water, the main water mass of the OMZ, south of the region where the nitrogen loss takes place.
3. Nitrogen cycling Our understanding of the marine nitrogen cycle, particularly in OMZs, has changed significantly in the recent years. Although some studies from the late 1950s and 1960s suggested that the anaerobic oxidation of ammonium could contribute to the N loss, until recently (heterotrophic) denitrification was considered to be
the only process by which N was lost as N2 from the ocean. Anaerobic ammonium oxidation with nitrate/nitrite (anammox) was discovered in 1995 in a waste-water treatment plant (Mulder et al., 1995) and, less than 10 years ago, anammox was reported to occur in natural systems (Thamdrup and Dalsgaard, 2002; Dalsgaard et al., 2003; Kuypers et al., 2003, 2005) and, less than 5 years ago in oceanic OMZs (Thamdrup et al., 2006; Hamersley et al., 2007). However, the details of the anammox bacteria distribution, dynamics, and ecological and biogeochemical importance are still largely unknown. Gala´n et al. (2009) present results on the phylogenetic diversity, vertical distribution, and activity of anammox bacteria off northern Chile, where anammox was first reported for the OMZ of the eastern Pacific (Thamdrup et al., 2006). Gala´n et al. found that microdiversity in anammox bacteria is higher than previously reported, and they describe a new phylogenetic lineage within the marine representatives of these microorganisms. Similar results have been reported recently for off Peru and the Arabian Sea (Woebken et al., 2008). Gala´n et al. also quantify the abundance, vertical distribution, and activity of these bacteria, revealing a peak in the upper part of the OMZ, probably associated with the intensification of biogeochemical cycling in this layer. Prior to the discovery of anammox, the biological oxidation of ammonium was thought to be carried out exclusively by aerobic ammonia-oxidizing bacteria during nitrification. Moreover, since this is a process that requires oxygen, it was assumed that nitrification would only be important at the oxyclines and not in the OMZ cores (Anderson et al., 1982). However, molecular studies have shown the presence of ammonia-oxidizing bacteria genes both in surface oxic waters and within the OMZ in the region (Molina et al., 2007). Molina and Farı´as (2009) show that nitrification rates are high enough to contribute significantly to ammonium oxidation and dark carbon fixation, not only at the oxycline but also within the OMZ. As nitrate is used, either partially or completely, in assimilatory or dissimilatory processes, it becomes enriched in 15N. This stable N isotope is heavier and much less abundant since biological processes preferentially utilize the lighter 14N. Thus, the 15N/14N ratio in nitrate and in organic matter relative to that in the
Fig. 1. (A) Distribution of the volume of the global ocean as a function of the dissolved oxygen content. (B) Cumulative volume frequency for the oxygen concentration. The gray box represents the percentage of waters with p10 mM dissolved oxygen and the white box the percentage of waters with p20 mM. Data come from the World Ocean Atlas 2001.
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atmospheric N2 (expressed as d15N) tells us something about the dominant nitrogen process operating in the ocean. In OMZs, subsurface nitrate reduction by microbial processes should leave a clear signal in the d15N of the nitrate that can then be transferred to the sediments if the nitrate is completely used by phytoplankton at the surface. However, the incomplete utilization of nitrate at the surface, the presence of other processes affecting the d15N (e.g. N2 fixation), and the advection of water masses through currents make the interpretation of observations less straightforward. De Pol-Holz et al. (2009) analyzed the sedimentary and water-column stable N isotope signal, showing a strong latitudinal gradient in sedimentary d15N that increases toward the northern Chilean coast. They infer that the d15N in sediments off Chile is controlled mainly by phytoplankton assimilation south of 411S, and by denitrification north of 301S. Moreover, they provide some isotopic evidence for the occurrence of N2 fixation in the water column of the OMZ, a process not known to occur in such waters.
4. Organic geochemistry Although there is no doubt that oxygenation levels affect the overall degradation of organic matter, the exact role of oxygen is still unknown (e.g., Westrich and Berner, 1984; Henrichs and Reeburgh, 1987; Canfield, 1989). The anaerobic degradation of organic matter is generally assumed to be slower than microbial aerobic degradation, mostly because organic matter is abundant in continental margin deposits underlying anoxic waters and the energy yield by anaerobic processes is lower than that of aerobic ones. To evaluate the degradation kinetics of labile organic matter under oxygenated and low-oxygen conditions, Pantoja et al. (2004) carried out a sediment trap experiment in the OMZ off northern Chile, finding that more than 80% of the protein sinking out of the 30-m horizon degraded between 30 and 300 m, i.e., within the suboxic zone. This fraction was similar to that which was degraded in the oxygenated top 30 m of the water column. Moreover, rate constants were in the same range for protein decay, regardless of dissolved oxygen. These authors concluded that particulate protein degradation is not affected by suboxic conditions in the water column, consistent with a degradation model of particulate protein controlled by extracellular microbial hydrolysis and not dependent on O2 availability. This matter was further investigated by Pantoja et al. (2009), in a study of macromolecular breakdown and monomer uptake in oxygenated and low-oxygen waters of the OMZ off northern Chile. These authors found similar microbial degradation rates for labile dissolved organic matter in oxic and suboxic waters off northern Chile, resulting in the processing of about 10 ton of peptide carbon per hour in the oxygen minimum layer. Espinosa et al. (2009) analyzed the bacterial phospholipidderived fatty acid methyl esters in suspended particulate matter in the water column off northern Chile, using capillary gas chromatography–mass spectrometry to elucidate the potential segregation of functional bacterial groups. Surprisingly, the vertical distribution of fatty acid methyl esters off Antofagasta did not reveal segregated zones of microbial activity, possibly because of the changing environment characterized by winddriven coastal upwelling that homogenizes different functional bacteria groups. In particular, the vertical distribution of lipid biomarkers in the water column off northern Chile showed that lipid biomarkers of sulfate-reducing bacteria are not only confined within the OMZ. This homogeneity could result from the vertical mixing produced by the transport of subsurface, nutrient-rich, CO2-saturated cold waters (Morales and Lange, 2004) that advect living biomass and detrital biogenic particles upward and off-
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shore, similar to that described for the Arabian Sea (Wakeham et al., 2002).
5. Plankton Recently planktonic archaea have been shown to be one of the most abundant unicellular microorganisms in the oceans. Until now, no information was available about the contribution of this group to the prokaryote assemblages inhabiting the eastern ˜ ones et al. (2009) used quantitative dot South Pacific Ocean. Quin blot 16S-rRNA hybridizations to estimate the relative abundance and vertical distribution of planktonic archaea of northern and central-southern Chile. They found that archaea make up 6–87% of the prokaryote rRNA in the water column without clear evidence of any seasonal pattern. Archaeal relative abundance was usually greater in the deeper layer (450 m), with contributions reaching up to 90% of the prokaryote rRNA; crenarchaeota appeared to be the most abundant archaeal group in the study area. These results indicate that archaea are an important fraction of the marine microbial community in the water column of the region, especially in the OMZ. The presence of subsurface oxygen-deficient waters has been shown to be a constraint for the vertical distribution of important zooplankton species and fishes in the region (Morales et al., 1996; Escribano, 1998; Giesecke and Gonza´lez, 2004). However, zooplankton species are known to be present and active within the OMZ (Hidalgo et al., 2005). Escribano et al. (2009) identified the main zooplankton species, among them the endemic copepod Eucalanus inermis and the abundant, also endemic, euphausid Euphausia mucronata, which live in close association with the OMZ. Escribano et al. also suggest that vertical migrations in and out of the OMZ by some of these species, particularly E. mucronata, contribute significantly to the carbon economy of the subsurface, low-oxygen waters. ˜ ones A different approach was taken by Gonza´lez and Quin (2009), who addressed the issues of spatial patterns of biomass and activity in the marine ecosystem. They used an ataxonomic approach based on enzymatic activity to show potential enzymatic activities involved in catabolic pathways in the OMZ. Of the analyzed enzymes, malate dehydrogenase had the highest oxidizing capability and was suggested as an indicator of microplanktonic catabolism in the OMZ.
6. Sea floor Benthic communities in oxygen-deficient regions are characterized by the presence of a limited numbers of macroand megafauna and abundant large sulfur-oxidizing bacteria and meiofauna (Levin, 2003). Veit-Ko¨hlera et al. (2009) analyzed the composition and abundance of the meiofauna found at four stations along the Chilean continental margin with different oxygen levels. As shown in previous studies, nematodes dominated this faunal size class. However, unlike previous observations that showed an inverse relationship between oxygen levels and meiofauna abundance, the highest abundance was not found at the permanent, most oxygen-poor station off northern Chile, but rather at a more southern station that presented seasonal oxygen deficiency. Clearly, oxygen is not the only variable determining the meiofauna abundance, and variations in oxygen availability over time should also be considered. On the other hand, Quiroga et al. (2009) present the distribution of benthic megafaunal and demersal fish assemblages at depths ranging from 120 to 2201 m (among the deepest ever taken in Chilean waters), reporting 147 species, mainly decapod
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crustaceans, gastropods, ophiuroids, asteroids, polychaetes, and demersal fishes. This analysis shows that water depth and dissolved oxygen levels are the main factors controlling megafaunal distributions along the continental shelf and in bathyal areas. Oxygen minimum zones are not static features in the ocean but vary on different temporal and spatial scales. In the region, important variations, ranging from intraseasonal to millennial, have already been recognized (Morales et al., 1999; Ulloa et al., 2001; De Pol-Holz et al., 2006, 2007). However, the ways in which such variability affect marine populations—particularly those of commercial importance—are largely unknown. The analysis of the sedimentary record may allow a reconstruction of the history of fish abundance and provide information on oxygenation conditions that can be related to variations in the preservation of certain components. Dı´az-Ochoa et al. (2009) studied the preservation of fish scales in the sedimentary record as a function of changing redox conditions over the last 700 years on the continental shelf off Callao, Peru. The record was dominated by scales of the anchovy Engraulis ringens followed by those of the hake Merluccius gayii. Their results indicate that the continental shelf underwent an abrupt shift to a less-oxygenated state in the early 19th century.
6.1. The future In the current climate-change scenario, the expansion of oceanic low-oxygen waters suggested by models (Keeling and Garcia, 2002) and recent observations in the eastern tropical Atlantic and the equatorial Pacific (Stramma et al., 2008) may be impacting the OMZs. Thus, the changes observed when using different historical data sets may be partly due to secular trends. Since the expansion and/or intensification of OMZs can significantly affect the biology, biogeochemical cycles, and even climate, there is a clear need to determine the seasonal to decadal timescale variations of dissolved oxygen in the subsurface of the ocean on a global scale. The incorporation of oxygen sensors into platforms such as profiling floats, gliders, and moorings (e.g., http://omz.udec.cl) should be encouraged and supported. Likewise, indicators of anaerobic metabolisms, such as those obtained with the enzymological approach presented by Gonza´lez ˜ ones (2009), will provide useful information as to the and Quin expansion and metabolic capabilities of organisms inhabiting low-oxygen waters. Although OMZs are recognized regions of global nitrogen sinks, the relative contribution of heterotrophic denitrification versus anammox is still not resolved. Anammox can help explain the near absence of ammonium in OMZ waters, and clearly contributes to the N2 lost there, but it does not explain the distribution and cycling of N2O (Castro-Gonza´lez and Farı´as, 2004; Farı´as et al., 2007, 2009), nor the presence of a high diversity of genes involved in conventional denitrification (Castro-Gonza´lez et al., 2005). Moreover, recent model results have suggested that these regions could also play a significant role in the global fixation of atmospheric N2 (Deutsch et al., 2007). Thus, much is still to be learned about nitrogen cycling in OMZs. Similarly, the role of OMZs in the global carbon cycle poses several questions; for instance, if anammox is responsible for an important fraction of N2 production, then how is organic matter being respired if denitrification is less important than assumed? In spite of their biogeochemical importance, the ecology and diversity of microorganisms present in OMZ waters is largely unknown. For example, a recent study suggested that pelagic sulfur-oxidizing bacteria should be main players in these systems (Stevens and Ulloa, 2008), although an active sulfur cycle is
usually not considered to be important in oceanic oxygendeficient waters. Similarly, the presence of lipid biomarkers of sulfate-reducing bacteria in the water column (Espinosa et al., 2009) suggests that those microorganisms are present and active, but no information is available on their abundance or metabolic rates. Furthermore, although the presence of archaea is just being ˜ ones et al., 2009), their diversity, revealed for the region (Quin ecology, and biogeochemical role in OMZ waters, as well as those of protists, have not yet been assessed. Most information on carbon degradation rates and fluxes in OMZ waters has been collected using bulk or labile (fresh) microbial substrates, but little is known on the diagenesis of more refractory materials that may be controlled by the availability of microorganisms. This aspect calls for the need to investigate the biogeochemical role of microorganisms inhabiting the OMZ. The biological diversity we are uncovering must have a biogeochemical meaning in this low-oxygen environment. The occurrence of permanent or temporal macrobiota, both in the sediments and in the water column of OMZs also requires future attention, not only in terms of diversity, life cycles, and metabolic/genetic adaptations to low-oxygen conditions—all largely unknown—but also in terms of their biogeochemical roles. Moreover, some of the species living in the region contribute to the largest pelagic fisheries of the world. The role that the OMZ plays and has played in their variability has largely been ignored. These research areas are but a few to which this collection of articles points the way for future studies of this fascinating ecosystem.
Acknowledgments We are very grateful to Danielle Barriga for her excellent work as the assistant to the Guest Editors. We also thank the Chief Editor of Deep-Sea Research II, John Milliman, for his continuous support, and Eric Galbraith (Princeton University) for providing the binned data that went into Fig. 1. This special issue was funded by the Chilean Commission for Scientific and Technological Research (CONICYT) through the FONDAP Program. References Anderson, J.J., Okubo, A., Robbins, A.S., Richards, F.A., 1982. A model for nitrite and nitrate distribution in oceanic oxygen minimum zones. Deep-Sea Research 29, 1113–1140. Canfield, D.E., 1989. Sulfate reduction and oxic respiration in marine sediments: implications for organic carbon preservation in euxinic environments. DeepSea Research 36, 121–138. Castro-Gonza´lez, M., Farı´as, L., 2004. N2O cycling at the core of oxygen minimum zone off northern Chile. Marine Ecology Progress Series 280, 1–11. Castro-Gonza´lez, M., Braker, G., Farı´as, L., Ulloa, O., 2005. Communities of nirS-type denitrifiers in the water column of the oxygen minimum zone in the eastern South Pacific. Environmental Microbiology 7, 1298–1306. ˜ a-Gonza´lez, J., 2003. N2 Dalsgaard, T., Canfield, D.E., Petersen, J., Thamdrup, B., Acun production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422, 606–608. De Pol-Holz, R., Ulloa, O., Dezileau, L., Kaiser, J., Lamy, F., Hebbeln, D., 2006. Melting of the Patagonian Ice Sheet and deglacial perturbatios of the nitrogen cycle in the eastern South Pacific. Geophysical Research Letters 33, L04704, doi:10. 1029/2005GL024477. De Pol-Holz, R., Ulloa, O., Lamy, F., Dezileau, L., Sabatier, P., Hebbeln, D., 2007. Late Quaternary variability of sedimentary nitrogen isotopes in the eastern South Pacific Ocean. Paleoceanography 22, PA2207, doi:10.1029/2006PA001308. De Pol-Holz, R., Robinson, R.S., Hebbeln, D., Sigman, D.M., Ulloa, O., 2009. Controls on sedimentary nitrogen isotopes along the Chile margin. Deep-Sea Research II, this issue [doi:10.1016/j.dsr2.2008.09.014]. Deutsch, C., Sarmiento, J.L., Sigman, D.M., Gruber, N., Dunne, J.P., 2007. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445, 163–167. ˜ oz, P., Dı´az-Ochoa, J.A., Lange, C.B., Pantoja, S., De Lange, G.J., Gutie´rrez, D., Mun Salamanca, M., 2009. Fish scales in sediments from off Callao, central Peru. Deep-Sea Resarch II, this issue [doi:10.1016/j.dsr2.2008.09.015]. Escribano, R., 1998. Population dynamics of Calanus chilensis in the Chilean eastern boundary Humboldt Current. Fisheries Oceanography 7, 245–251.
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Contents lists available at ScienceDirect
Deep-Sea Research II journal homepage: www.elsevier.com/locate/dsr2
The oxygen minimum zone of the eastern South Pacific Osvaldo Ulloa , Silvio Pantoja ´fica en el Pacı´fico Sur-oriental, Universidad de Concepcio ´n Oceanogra ´n, Casilla 160-C, Concepcio ´n, Chile Departamento de Oceanografı´a and Centro de Investigacio
a r t i c l e in fo
abstract
Available online 10 December 2008
In spite of the fact that oxygen-deficient waters with p20 mM of dissolved oxygen—known as oxygen minimum zones (OMZs)—occupy only 1% of the volume of the global ocean, they disproportionately affect global biogeochemical cycles, particularly the nitrogen cycle. The macrobiota diversity in OMZs is low, but the fauna that do inhabit these regions present special adaptations to the low-oxygen conditions. Conversely, microbial communities in the OMZ water column and sediments are abundant and phylogenetically and metabolically very diverse, and microbial processes occurring therein (e.g., denitrification, anammox, and organic matter degradation) are important for global marine biogeochemical cycles. In this introductory article, we present the collection of papers for the special volume on the OMZ of the eastern South Pacific, one of the three main open-ocean oxygen-deficient regions of the global ocean. These papers deal with aspects of regional oceanography, inorganic and organic geochemistry, ecology, and the biochemistry of micro and macro organisms—both in the plankton and in the sediments—and past changes in the fish scales preserved in the sediments bathed by OMZ waters. & 2008 Elsevier Ltd. All rights reserved.
Keywords: Oxygen minimum zone Biogeochemical cycling Microbial communities Plankton Benthos Fish scales
1. Introduction Oxygen is a key element for biology and the cycling of geochemical elements, and has shaped the chemical and biological evolution on Earth. Oxygen accounts for 21% of the volume in the atmosphere and is the most thermodynamically favorable terminal electron acceptor for organic matter oxidation, making it the current main oxidant for the energetic demands of the biosphere. However, exceptions to this can be found in the soils, ocean sediments, anoxic water bodies, and certain compartments in living organisms (e.g., digestive tracks) that are restricted from a sufficient supply of dissolved oxygen to compensate for its lost by aerobic respiration. Because of the thermohaline circulation, oxygen penetrates the deepest waters of the global ocean, including the abyssal plains and trenches. However, due to the respiration of the organic matter produced in the lighted surface layer as it settles down through the water column and the nature of global deep circulation, the oxygen concentrations in intermediate waters (100–1000 m deep) are lower than in the surface waters above and deep waters below (Wyrtki, 1962). Moreover, in some regions, upwelling, sluggish circulation, and high primary productivity in surface waters cause oxygen concentrations in subsurface waters to drop to levels o20 mM and possibly even to anoxia; these permanently low-oxygen regions are known as oxygen minimum zones (OMZs). These features occur in large open-ocean areas of
the eastern tropical Pacific Ocean and the northern reaches of the tropical Indian Ocean (Kamykowski and Zentara, 1990). OMZ waters also impinge on the sea floor of continental margins (Helly and Levin, 2004). These areas have low biodiversity of macrofauna, and are inhospitable to most commercially valuable marine resources. However, OMZs support benthic communities that include conspicuously large sulfur-oxidizing bacteria, nitrate-respiring protists, and metazoans adapted to oxygen-deficient conditions (e.g., Gallardo, 1977; Levin, 2003; Risgaard-Petersen et al., 2006). In March 2002, the Chilean government established the Center for Oceanographic Research in the eastern South Pacific (Centro de Investigacio´n Oceanogra´fica en el Pacı´fico Sur-Oriental, COPAS) at the Universidad de Concepcio´n (http://www.copas.udec.cl) as one of the country’s centers of excellence (Lange and Ulloa, 2003). From the beginning, one of the main research themes at COPAS has been the study of the structure and functioning of the OMZ in the eastern South Pacific. Several articles on the topic have been published elsewhere (see references), as have sets of articles on the oceanographic characteristics of the region (Morales and Lange, 2004; Escribano and Schneider, 2007). A collection of new articles dealing with the study of the OMZ is presented in this issue. The following provides a brief overview of some of the major highlight of the articles published herein.
2. Large-scale features Corresponding author. Tel.: +56 41 220 3585; fax: +56 41 223 9900.
E-mail address: [email protected] (O. Ulloa). 0967-0645/$ - see front matter & 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2008.12.004
According to the World Ocean Atlas 2001 (WOA01), waters with p20 mM of dissolved oxygen represent only 1% of the
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volume of the global ocean, whereas waters with p10 mM account for o0.3% (Fig. 1). However, as shown by Fuenzalida et al. (2009), estimates based on the WOA01 product may severely underestimate (up to 90%) the volume and area of the OMZ in the eastern South Pacific Ocean. This is probably also the case for the other OMZs. Part of the problem lies in the density of data from the region that went into producing the WOA01. Another problem, as discussed by Fuenzalida et al., is the way in which the WOA01 are processed, using 33 standard depths to obtain the gridded climatologies versus the quasi-continuous modern data obtained with conductivity-temperature-depth-oxygen (CTDO) profilers. Apart from the low-oxygen concentrations, a characteristic feature of OMZs is the presence of an inorganic nitrogen (N) deficit relative to inorganic phosphorus (P). As organic matter produced at the surface with a relatively fixed ratio of nitrogen to phosphorus (the Redfield ratio) sinks and becomes mineralized, N and P are released in the same proportion, such that the concentrations of inorganic N and P in the ocean are close to the molar ratio in organic matter (16:1); this is the case in most of the global ocean. However, in OMZs, nitrogen is lost primarily as N2 through heterotrophic denitrification and anammox (see the next section), so that the concentration of inorganic nitrogen (mainly nitrate+nitrite) deviates significantly from the Redfield ratio and can be quantified as a nitrogen deficit. Silva et al. (2009) used historical data collected from 101 to 501S and from the South American west coast to 1001W to describe the main physical and chemical characteristics of the water masses in the region. They also used the nitrate deficit as chemical marker to trace Equatorial Subsurface Water, the main water mass of the OMZ, south of the region where the nitrogen loss takes place.
3. Nitrogen cycling Our understanding of the marine nitrogen cycle, particularly in OMZs, has changed significantly in the recent years. Although some studies from the late 1950s and 1960s suggested that the anaerobic oxidation of ammonium could contribute to the N loss, until recently (heterotrophic) denitrification was considered to be
the only process by which N was lost as N2 from the ocean. Anaerobic ammonium oxidation with nitrate/nitrite (anammox) was discovered in 1995 in a waste-water treatment plant (Mulder et al., 1995) and, less than 10 years ago, anammox was reported to occur in natural systems (Thamdrup and Dalsgaard, 2002; Dalsgaard et al., 2003; Kuypers et al., 2003, 2005) and, less than 5 years ago in oceanic OMZs (Thamdrup et al., 2006; Hamersley et al., 2007). However, the details of the anammox bacteria distribution, dynamics, and ecological and biogeochemical importance are still largely unknown. Gala´n et al. (2009) present results on the phylogenetic diversity, vertical distribution, and activity of anammox bacteria off northern Chile, where anammox was first reported for the OMZ of the eastern Pacific (Thamdrup et al., 2006). Gala´n et al. found that microdiversity in anammox bacteria is higher than previously reported, and they describe a new phylogenetic lineage within the marine representatives of these microorganisms. Similar results have been reported recently for off Peru and the Arabian Sea (Woebken et al., 2008). Gala´n et al. also quantify the abundance, vertical distribution, and activity of these bacteria, revealing a peak in the upper part of the OMZ, probably associated with the intensification of biogeochemical cycling in this layer. Prior to the discovery of anammox, the biological oxidation of ammonium was thought to be carried out exclusively by aerobic ammonia-oxidizing bacteria during nitrification. Moreover, since this is a process that requires oxygen, it was assumed that nitrification would only be important at the oxyclines and not in the OMZ cores (Anderson et al., 1982). However, molecular studies have shown the presence of ammonia-oxidizing bacteria genes both in surface oxic waters and within the OMZ in the region (Molina et al., 2007). Molina and Farı´as (2009) show that nitrification rates are high enough to contribute significantly to ammonium oxidation and dark carbon fixation, not only at the oxycline but also within the OMZ. As nitrate is used, either partially or completely, in assimilatory or dissimilatory processes, it becomes enriched in 15N. This stable N isotope is heavier and much less abundant since biological processes preferentially utilize the lighter 14N. Thus, the 15N/14N ratio in nitrate and in organic matter relative to that in the
Fig. 1. (A) Distribution of the volume of the global ocean as a function of the dissolved oxygen content. (B) Cumulative volume frequency for the oxygen concentration. The gray box represents the percentage of waters with p10 mM dissolved oxygen and the white box the percentage of waters with p20 mM. Data come from the World Ocean Atlas 2001.
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atmospheric N2 (expressed as d15N) tells us something about the dominant nitrogen process operating in the ocean. In OMZs, subsurface nitrate reduction by microbial processes should leave a clear signal in the d15N of the nitrate that can then be transferred to the sediments if the nitrate is completely used by phytoplankton at the surface. However, the incomplete utilization of nitrate at the surface, the presence of other processes affecting the d15N (e.g. N2 fixation), and the advection of water masses through currents make the interpretation of observations less straightforward. De Pol-Holz et al. (2009) analyzed the sedimentary and water-column stable N isotope signal, showing a strong latitudinal gradient in sedimentary d15N that increases toward the northern Chilean coast. They infer that the d15N in sediments off Chile is controlled mainly by phytoplankton assimilation south of 411S, and by denitrification north of 301S. Moreover, they provide some isotopic evidence for the occurrence of N2 fixation in the water column of the OMZ, a process not known to occur in such waters.
4. Organic geochemistry Although there is no doubt that oxygenation levels affect the overall degradation of organic matter, the exact role of oxygen is still unknown (e.g., Westrich and Berner, 1984; Henrichs and Reeburgh, 1987; Canfield, 1989). The anaerobic degradation of organic matter is generally assumed to be slower than microbial aerobic degradation, mostly because organic matter is abundant in continental margin deposits underlying anoxic waters and the energy yield by anaerobic processes is lower than that of aerobic ones. To evaluate the degradation kinetics of labile organic matter under oxygenated and low-oxygen conditions, Pantoja et al. (2004) carried out a sediment trap experiment in the OMZ off northern Chile, finding that more than 80% of the protein sinking out of the 30-m horizon degraded between 30 and 300 m, i.e., within the suboxic zone. This fraction was similar to that which was degraded in the oxygenated top 30 m of the water column. Moreover, rate constants were in the same range for protein decay, regardless of dissolved oxygen. These authors concluded that particulate protein degradation is not affected by suboxic conditions in the water column, consistent with a degradation model of particulate protein controlled by extracellular microbial hydrolysis and not dependent on O2 availability. This matter was further investigated by Pantoja et al. (2009), in a study of macromolecular breakdown and monomer uptake in oxygenated and low-oxygen waters of the OMZ off northern Chile. These authors found similar microbial degradation rates for labile dissolved organic matter in oxic and suboxic waters off northern Chile, resulting in the processing of about 10 ton of peptide carbon per hour in the oxygen minimum layer. Espinosa et al. (2009) analyzed the bacterial phospholipidderived fatty acid methyl esters in suspended particulate matter in the water column off northern Chile, using capillary gas chromatography–mass spectrometry to elucidate the potential segregation of functional bacterial groups. Surprisingly, the vertical distribution of fatty acid methyl esters off Antofagasta did not reveal segregated zones of microbial activity, possibly because of the changing environment characterized by winddriven coastal upwelling that homogenizes different functional bacteria groups. In particular, the vertical distribution of lipid biomarkers in the water column off northern Chile showed that lipid biomarkers of sulfate-reducing bacteria are not only confined within the OMZ. This homogeneity could result from the vertical mixing produced by the transport of subsurface, nutrient-rich, CO2-saturated cold waters (Morales and Lange, 2004) that advect living biomass and detrital biogenic particles upward and off-
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shore, similar to that described for the Arabian Sea (Wakeham et al., 2002).
5. Plankton Recently planktonic archaea have been shown to be one of the most abundant unicellular microorganisms in the oceans. Until now, no information was available about the contribution of this group to the prokaryote assemblages inhabiting the eastern ˜ ones et al. (2009) used quantitative dot South Pacific Ocean. Quin blot 16S-rRNA hybridizations to estimate the relative abundance and vertical distribution of planktonic archaea of northern and central-southern Chile. They found that archaea make up 6–87% of the prokaryote rRNA in the water column without clear evidence of any seasonal pattern. Archaeal relative abundance was usually greater in the deeper layer (450 m), with contributions reaching up to 90% of the prokaryote rRNA; crenarchaeota appeared to be the most abundant archaeal group in the study area. These results indicate that archaea are an important fraction of the marine microbial community in the water column of the region, especially in the OMZ. The presence of subsurface oxygen-deficient waters has been shown to be a constraint for the vertical distribution of important zooplankton species and fishes in the region (Morales et al., 1996; Escribano, 1998; Giesecke and Gonza´lez, 2004). However, zooplankton species are known to be present and active within the OMZ (Hidalgo et al., 2005). Escribano et al. (2009) identified the main zooplankton species, among them the endemic copepod Eucalanus inermis and the abundant, also endemic, euphausid Euphausia mucronata, which live in close association with the OMZ. Escribano et al. also suggest that vertical migrations in and out of the OMZ by some of these species, particularly E. mucronata, contribute significantly to the carbon economy of the subsurface, low-oxygen waters. ˜ ones A different approach was taken by Gonza´lez and Quin (2009), who addressed the issues of spatial patterns of biomass and activity in the marine ecosystem. They used an ataxonomic approach based on enzymatic activity to show potential enzymatic activities involved in catabolic pathways in the OMZ. Of the analyzed enzymes, malate dehydrogenase had the highest oxidizing capability and was suggested as an indicator of microplanktonic catabolism in the OMZ.
6. Sea floor Benthic communities in oxygen-deficient regions are characterized by the presence of a limited numbers of macroand megafauna and abundant large sulfur-oxidizing bacteria and meiofauna (Levin, 2003). Veit-Ko¨hlera et al. (2009) analyzed the composition and abundance of the meiofauna found at four stations along the Chilean continental margin with different oxygen levels. As shown in previous studies, nematodes dominated this faunal size class. However, unlike previous observations that showed an inverse relationship between oxygen levels and meiofauna abundance, the highest abundance was not found at the permanent, most oxygen-poor station off northern Chile, but rather at a more southern station that presented seasonal oxygen deficiency. Clearly, oxygen is not the only variable determining the meiofauna abundance, and variations in oxygen availability over time should also be considered. On the other hand, Quiroga et al. (2009) present the distribution of benthic megafaunal and demersal fish assemblages at depths ranging from 120 to 2201 m (among the deepest ever taken in Chilean waters), reporting 147 species, mainly decapod
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crustaceans, gastropods, ophiuroids, asteroids, polychaetes, and demersal fishes. This analysis shows that water depth and dissolved oxygen levels are the main factors controlling megafaunal distributions along the continental shelf and in bathyal areas. Oxygen minimum zones are not static features in the ocean but vary on different temporal and spatial scales. In the region, important variations, ranging from intraseasonal to millennial, have already been recognized (Morales et al., 1999; Ulloa et al., 2001; De Pol-Holz et al., 2006, 2007). However, the ways in which such variability affect marine populations—particularly those of commercial importance—are largely unknown. The analysis of the sedimentary record may allow a reconstruction of the history of fish abundance and provide information on oxygenation conditions that can be related to variations in the preservation of certain components. Dı´az-Ochoa et al. (2009) studied the preservation of fish scales in the sedimentary record as a function of changing redox conditions over the last 700 years on the continental shelf off Callao, Peru. The record was dominated by scales of the anchovy Engraulis ringens followed by those of the hake Merluccius gayii. Their results indicate that the continental shelf underwent an abrupt shift to a less-oxygenated state in the early 19th century.
6.1. The future In the current climate-change scenario, the expansion of oceanic low-oxygen waters suggested by models (Keeling and Garcia, 2002) and recent observations in the eastern tropical Atlantic and the equatorial Pacific (Stramma et al., 2008) may be impacting the OMZs. Thus, the changes observed when using different historical data sets may be partly due to secular trends. Since the expansion and/or intensification of OMZs can significantly affect the biology, biogeochemical cycles, and even climate, there is a clear need to determine the seasonal to decadal timescale variations of dissolved oxygen in the subsurface of the ocean on a global scale. The incorporation of oxygen sensors into platforms such as profiling floats, gliders, and moorings (e.g., http://omz.udec.cl) should be encouraged and supported. Likewise, indicators of anaerobic metabolisms, such as those obtained with the enzymological approach presented by Gonza´lez ˜ ones (2009), will provide useful information as to the and Quin expansion and metabolic capabilities of organisms inhabiting low-oxygen waters. Although OMZs are recognized regions of global nitrogen sinks, the relative contribution of heterotrophic denitrification versus anammox is still not resolved. Anammox can help explain the near absence of ammonium in OMZ waters, and clearly contributes to the N2 lost there, but it does not explain the distribution and cycling of N2O (Castro-Gonza´lez and Farı´as, 2004; Farı´as et al., 2007, 2009), nor the presence of a high diversity of genes involved in conventional denitrification (Castro-Gonza´lez et al., 2005). Moreover, recent model results have suggested that these regions could also play a significant role in the global fixation of atmospheric N2 (Deutsch et al., 2007). Thus, much is still to be learned about nitrogen cycling in OMZs. Similarly, the role of OMZs in the global carbon cycle poses several questions; for instance, if anammox is responsible for an important fraction of N2 production, then how is organic matter being respired if denitrification is less important than assumed? In spite of their biogeochemical importance, the ecology and diversity of microorganisms present in OMZ waters is largely unknown. For example, a recent study suggested that pelagic sulfur-oxidizing bacteria should be main players in these systems (Stevens and Ulloa, 2008), although an active sulfur cycle is
usually not considered to be important in oceanic oxygendeficient waters. Similarly, the presence of lipid biomarkers of sulfate-reducing bacteria in the water column (Espinosa et al., 2009) suggests that those microorganisms are present and active, but no information is available on their abundance or metabolic rates. Furthermore, although the presence of archaea is just being ˜ ones et al., 2009), their diversity, revealed for the region (Quin ecology, and biogeochemical role in OMZ waters, as well as those of protists, have not yet been assessed. Most information on carbon degradation rates and fluxes in OMZ waters has been collected using bulk or labile (fresh) microbial substrates, but little is known on the diagenesis of more refractory materials that may be controlled by the availability of microorganisms. This aspect calls for the need to investigate the biogeochemical role of microorganisms inhabiting the OMZ. The biological diversity we are uncovering must have a biogeochemical meaning in this low-oxygen environment. The occurrence of permanent or temporal macrobiota, both in the sediments and in the water column of OMZs also requires future attention, not only in terms of diversity, life cycles, and metabolic/genetic adaptations to low-oxygen conditions—all largely unknown—but also in terms of their biogeochemical roles. Moreover, some of the species living in the region contribute to the largest pelagic fisheries of the world. The role that the OMZ plays and has played in their variability has largely been ignored. These research areas are but a few to which this collection of articles points the way for future studies of this fascinating ecosystem.
Acknowledgments We are very grateful to Danielle Barriga for her excellent work as the assistant to the Guest Editors. We also thank the Chief Editor of Deep-Sea Research II, John Milliman, for his continuous support, and Eric Galbraith (Princeton University) for providing the binned data that went into Fig. 1. This special issue was funded by the Chilean Commission for Scientific and Technological Research (CONICYT) through the FONDAP Program. References Anderson, J.J., Okubo, A., Robbins, A.S., Richards, F.A., 1982. A model for nitrite and nitrate distribution in oceanic oxygen minimum zones. Deep-Sea Research 29, 1113–1140. Canfield, D.E., 1989. Sulfate reduction and oxic respiration in marine sediments: implications for organic carbon preservation in euxinic environments. DeepSea Research 36, 121–138. Castro-Gonza´lez, M., Farı´as, L., 2004. N2O cycling at the core of oxygen minimum zone off northern Chile. Marine Ecology Progress Series 280, 1–11. Castro-Gonza´lez, M., Braker, G., Farı´as, L., Ulloa, O., 2005. Communities of nirS-type denitrifiers in the water column of the oxygen minimum zone in the eastern South Pacific. Environmental Microbiology 7, 1298–1306. ˜ a-Gonza´lez, J., 2003. N2 Dalsgaard, T., Canfield, D.E., Petersen, J., Thamdrup, B., Acun production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422, 606–608. De Pol-Holz, R., Ulloa, O., Dezileau, L., Kaiser, J., Lamy, F., Hebbeln, D., 2006. Melting of the Patagonian Ice Sheet and deglacial perturbatios of the nitrogen cycle in the eastern South Pacific. Geophysical Research Letters 33, L04704, doi:10. 1029/2005GL024477. De Pol-Holz, R., Ulloa, O., Lamy, F., Dezileau, L., Sabatier, P., Hebbeln, D., 2007. Late Quaternary variability of sedimentary nitrogen isotopes in the eastern South Pacific Ocean. Paleoceanography 22, PA2207, doi:10.1029/2006PA001308. De Pol-Holz, R., Robinson, R.S., Hebbeln, D., Sigman, D.M., Ulloa, O., 2009. Controls on sedimentary nitrogen isotopes along the Chile margin. Deep-Sea Research II, this issue [doi:10.1016/j.dsr2.2008.09.014]. Deutsch, C., Sarmiento, J.L., Sigman, D.M., Gruber, N., Dunne, J.P., 2007. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445, 163–167. ˜ oz, P., Dı´az-Ochoa, J.A., Lange, C.B., Pantoja, S., De Lange, G.J., Gutie´rrez, D., Mun Salamanca, M., 2009. Fish scales in sediments from off Callao, central Peru. Deep-Sea Resarch II, this issue [doi:10.1016/j.dsr2.2008.09.015]. Escribano, R., 1998. Population dynamics of Calanus chilensis in the Chilean eastern boundary Humboldt Current. Fisheries Oceanography 7, 245–251.
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